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Article

Predicting Cloned Disease Resistance Gene Homologs (CDRHs) in Radish, Underutilised Oilseeds, and Wild Brassicaceae Species

by
Aldrin Y. Cantila
,
William J. W. Thomas
,
Philipp E. Bayer
,
David Edwards
and
Jacqueline Batley
*
School of Biological Sciences, The University of Western Australia, Perth 6009, Australia
*
Author to whom correspondence should be addressed.
Plants 2022, 11(22), 3010; https://doi.org/10.3390/plants11223010
Submission received: 18 October 2022 / Revised: 1 November 2022 / Accepted: 2 November 2022 / Published: 8 November 2022
(This article belongs to the Special Issue Pre-breeding towards the Effective Utilization of Plant Genetic Resources Volume II)
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Abstract

:
Brassicaceae crops, including Brassica, Camelina and Raphanus species, are among the most economically important crops globally; however, their production is affected by several diseases. To predict cloned disease resistance (R) gene homologs (CDRHs), we used the protein sequences of 49 cloned R genes against fungal and bacterial diseases in Brassicaceae species. In this study, using 20 Brassicaceae genomes (17 wild and 3 domesticated species), 3172 resistance gene analogs (RGAs) (2062 nucleotide binding-site leucine-rich repeats (NLRs), 497 receptor-like protein kinases (RLKs) and 613 receptor-like proteins (RLPs)) were identified. CDRH clusters were also observed in Arabis alpina, Camelina sativa and Cardamine hirsuta with assigned chromosomes, consisting of 62 homogeneous (38 NLR, 17 RLK and 7 RLP clusters) and 10 heterogeneous RGA clusters. This study highlights the prevalence of CDRHs in the wild relatives of the Brassicaceae family, which may lay the foundation for rapid identification of functional genes and genomics-assisted breeding to develop improved disease-resistant Brassicaceae crop cultivars.

1. Introduction

The Brassicaceae family, also known as Cruciferae due to its cross-shape four-petal flower [1], is one of the most diverse and agronomically important plant families, consisting of 44 tribes, 372 genera and 4060 species [2,3]. The Brassica species (B. rapa, B. nigra, B. oleracea, B. juncea, B. napus and B. carinata), Camelina sativa, Raphanus sativus and Sinapis alba are crop members, which are produced for vegetables, edible oil, herbs, spices, condiments and fodder. The Brassicaceae also contains many model species that are used in various areas of research, including Arabidopsis thaliana for genetic studies [4], Arabidopsis halleri for heavy metal (e.g., cadmium and zinc) accumulation and tolerance [5], Arabis alpina in ecological studies [6], Barbarea vulgaris for insect resistance [7], Boechera species in apomixis research [8], Brassica species in crop evolution [9], C. sativa in metabolic oils [10], Cardamine hirsuta in leaf structure and morphology [11], Eutrema salsugineum in salinity stress [12] and Lepidium meyenii in floral structure [13]. In addition, species, such as Amoracia rusticana, Cheiranthes cheiri, Isatis tinctoria, Matthiola incana and Raphanus raphanistrum, have industrial uses (biofuels, dyes, etc.) [14,15,16,17,18], while species in the genera Aethionema, Cheiranthus, Erysimum, Hesperis, Iberis, Lobularia, Lunaria, Malcolmia and Matthiola are cultivated as ornamentals [19,20].
The production of Brassicaceae species, especially the crop members, is limited by various pathogens, such as Leptosphaeria species (L. maculans, L. biglobosa), Sclerotinia sclerotiorum, Albugo candida, Hyaloperonospora species (H. parasitica, H. arabidopsidis), Pseudomonas syringae, Plasmodiophora brassicae, Xanthomonas spp., Fusarium oxysporum matthioli, Botrytis cinerea, Erysiphe cichoracearum and Alternaria species (A. brassicicola, A. brassicae), which cause blackleg, Sclerotinia stem rot, white rust, downy mildew, bacterial leaf spot, clubroot, black rot, Fusarium wilt, grey mould, powdery mildew and Alternaria black spot diseases, respectively [21,22,23,24,25]. Crops have qualitative and quantitative disease resistance to overcome pathogens. The quantitative resistance, governed by many minor genes, is a partial resistance manifesting at later stages of the crop, while qualitative resistance, governed by major genes or resistance genes (R genes), is largely manifested from the early stages up to the maturity stage of the crop. Among the types of resistance in Brassicaceae crops, qualitative resistance is commonly used to screen lines in early stages of the genotypes for disease resistance breeding and development. For instance, a set of pathogen isolates containing avirulence (Avr) genes is used to screen white rust resistance in B. juncea genotypes [26] and blackleg resistance in B. napus genotypes [27,28] by assessing a hypersensitive response observed in the cotyledons. Clubroot resistance is also screened either in the cotyledon and roots of the seedlings in Brassicaceae species [29,30,31,32].
The crop wild relatives (CWRs) of the cultivated Brassicaceae species can be used to improve disease resistance by integrating favourable alleles harboured by the CWRs into the crop members. For example, Brassica fruticulosa and Erucastrum cardaminoides were introgressed, via wide hybridization, including chromosome doubling and bridging species, to B. juncea with disease R genes against Sclerotinia stem rot [33,34]. In addition, B. juncea-S. alba hybrids were developed through somatic hybridization, which leads to the transfer of Alternaria black spot disease resistance to B. juncea [35]. The wild C genome of Brassica incana was also introduced to B. napus through interspecific hybridization and pyramiding for Sclerotinia stem rot resistance [36], while Alternaria black spot and white rust resistance from the wild crucifers Diplotaxis erucoides and Brassica maurorum were introduced into B. rapa with the aid of sequential ovary-ovule culture [37]. Lastly, A. thaliana, B. insularis, B. atlantica, B. macrocarpa, Diplotaxis muralis, Eruca pinnatifia, Erucastrum gallicum, R. raphanistrum, Sinapsis arvensis, Sisymbrium loeselii and Thlaspi arvense have been found with proteins/compounds that may enhance blackleg resistance in B. napus [38,39,40,41,42,43,44,45].
Plant disease R genes, also called resistance-gene analogs (RGAs), play a significant role in triggering the genetic resistance-defence response in crops [46] and are grouped into three main classes: nucleotide-binding site (NBS)-leucine rich repeats (LRR) (NLRs), receptor-like protein kinases (RLKs) and receptor-like proteins (RLPs). NLRs, with the subclasses coiled-coil (CC)-NBS (CN), CNL, NBS, NBS-LRR (NL), Toll/Interleukin-1 receptor (TIR)-NBS-LRR (TNL), TIR-NBS (TN), TIR with unknown domains (TX), NLR with other domains (Other-NLR), are generally involved in effector-triggered plant immunity (ETI) and plant defence [47,48,49,50]. On the other hand, RLKs, with the subclasses, including LRR-RLK, Lysin motif (LsyM) (LysM-RLK) and other receptor (Other-RLK) [51] and RLPs, with the subclasses, including LRR-RLP and LysM (LysM-RLP), are not only involved in the first line of defence by recognising pathogen elicitors [52,53], but also in plant development [54,55].
This study aimed to determine what RGAs are homologous to cloned fungal and bacterial R genes across 20 Brassicaceae genomes and to assess the retention and diversification of RGA domains in the homologs and their physical clustering patterns.

2. Results

2.1. Prediction of RGAs in Brassica cretica, Capsella bursa-pastoris and Sinapis alba

RGAugury predicted a combined total of 3738 RGAs in B. cretica (982 RGAs; with 230 NLRs, 614 RLKs and 138 RLPs), C. bursa-pastoris (1474 RGAs; with 353 NLRs, 925 RLKs and 196 RLPs) and S. alba (1282 RGAs; with 208 NLRs, 943 RLKs and 131 RLPs) genomes (Figure 1, Table S1). Of these RGAs, 791 were NLRs (195 TNL, 161 NL, 161 TX, 110 CNL, 53 TN, 51 NBS, 26 CN and 34 Other-NLR), 2482 were RLKs (1486 Other-RLK, 982 LRR-RLK and 14 LysM-RLK) and 465 were RLPs (457 LRR-RLP and 8 LysM-RLP) (Figure 1).

2.2. Identification of CDRHs across the Study Species and Diseases

The 3172 cloned disease R gene homologs (CDRHs) identified were all RGAs: 2062 NLRs, 497 RLKs and 613 RLPs, with an average of 159 CDRHs (RGAs) in each of the 20 studied genomes/species (Figure 2, Table S2). C. sativa contained the highest number of CDRHs: 307, followed by Boechera stricta (296), C. hirsuta (240), A. alpina (226), C. bursa-pastoris (197), B. vulgaris (171) and Arabidopsis lyrata (162) (Figure 2). The rest of the studied Brassicaceae contained less than the average CDRHs per species, with the lowest in Schrenkiella parvula (62), Leavenworthia alabamica (91), Capsella rubella (94) and R. raphanistrum (99) (Figure 2). It should also be noted that A. lyrata, C. bursa-pastoris and R. sativus (135 CDRHs) had the highest number of CDRHs in their respective subfamilies (Figure 2).
The cloned R genes against bacterial leaf spot (At_ADR1, At_BAK1, At_FLS2, At_NDR1, At_NRG1a, At_NRG1b, At_PBS1, At_RLP30, At_RLP32, At_RPM1, At_RPS2, At_RPS4, At_RPS5, At_RRS1 and At_SOBIR1) had a total of 752 CDRHs (Figure 3). C. sativa had the highest number of CDRHs, 85, followed by 59 and 58 in C. hirsuta and L. meyenii, respectively (Figure 3). For the gene conferring resistance to another bacterial disease (black rot), At_RLP1, a total of 36 CDRHs were identified, with the highest numbers found in C. hirsuta and C. bursa-pastoris with 6 and 5, respectively (Figure 3).
In total, 921 CDRHs associated with cloned R genes against the fungal disease downey mildew (At_ADR1, At_NRG1a, At_NRG1b, At_RLP42, At_RPP1, At_RPP2a, At_RPP2B, At_RPP4, At_RPP5, At_RPP7, At_RPP8, At_RPP13 and At_RPP39) were identified (Figure 3). Of these, 89 and 86 CDRHs were the highest numbers obtained in C. sativa and B. stricta, respectively. The cloned R genes against white rust (Bju_WRR1, At_RAC1, At_WRR4a, At_WRR4b, At_WRR8, At_WRR9 and At_WRR12) (Table 1) were recorded having a total of 544 CDRHs (Figure 3). The highest count was found in B. stricta: 106 CDRHs, followed by A. alpina (52 CDRHs). For blackleg, the cloned R genes (Bna_MAPk, Bna_LepR3/Rlm2, Bna_Rlm9/4/7, At_RLM1a, At_RLM1b and At_RLM3) had a total of 509 CDRHs (Figure 3). Both A. alpina and B. stricta had the most CDRHs, with 49 each, followed by C. hirsuta with 44 and C. sativa with 40. For Sclerotinia stem rot, the cloned R genes (At_BAK1, At_RLP23, At_RLP30 and At_SOBIR1) had a total of 310 CDRHs with the highest count observed in C. sativa with 48 (Figure 3).
The cloned R genes (Bol_FocBo1, At_RFO1, At_RFO2 and At_RFO3) against Fusarium wilt had 283 CDRHs in total with the highest numbers being 38 (C. sativa) and 23 CDRHs (C. hirsuta and A. alpina) (Figure 3). The cloned R genes against grey mould (At_RLP42 and At_RLM3) had a total of 134 CDRHs with the highest CDRHs obtained in C. sativa (21 CDRHs), S. alba (13 CDRHs) and C. bursa-pastoris (13 CDRHs) (Figure 3). The cloned R genes (Bra_Crr1a and cRa/cRb) against clubroot had a total of 117 CDRHs with A. alpina and S. alba containing the highest counts with 17 and 12 CDRHs, respectively (Figure 3). At_ADR1 against powdery mildew had 45 CDRHs, with 7 CDRHs in C. sativa as the highest count. At_RLM3 conferring resistance to Alternaria black spot had 22 CDRHs with 2 CDRHs as the highest in each of eight species (A. alpina, B. stricta, B. vulgaris, C. bursa-pastoris, Capsella grandiflora, E. salsugineum, R. sativus and T. arvense) (Figure 3).

2.3. Retention and Diversification of RGA Domains in CDRHs

In terms of RGA subclasses, CDRHs were composed of 647 TNL, 613 LRR-RLP, 402 NL, 361 CNL, 301 Other-RLK, 271 TX, 196 LRR-RLK, 168 TN, 89 Other-NLR, 78 NBS and 46 CN (Figure 2), which shows the variation in CDRHs throughout the Brassicaceae family.
The RGA domain retention in the CDRHs (same RGA domain compared to its reference cloned R gene) and diversification (different RGA domain compared to its reference cloned R gene) were also noted in this study (Table 1). In total, 1992 (63%) and 1180 (37%) out of the 3172 CDRHs had retained and diversified their RGA domain compared to their reference cloned R gene, respectively (Table 1). It can be noted that the cloned R genes classed as Other-RLK had their corresponding CDRHs also classified as Other-RLK (100%, 298 out of 298 CDRHs). The next highest numbers retaining the same RGA domain were 98%, 95% and 61% in CDRHs from the LRR-RLK (167 out of 170 CDRHs), LRR-RLP (599 out of 628 CDRHs) and CNL (204 out of 332 CDRHs) cloned R genes, respectively. The remaining CDRHs from the NL, TNL and TN cloned R genes had 49% (115 out of 236 CDRHs), 45% (604 out of 1356 CDRHs) and 38% (5 out of 13 CDRHs) RGA domain retention, respectively.
The gene diversification could either be through truncation (one or two domains omitted), addition (one or two domains were added) or the combination of truncation and addition of RGA domains. Of the diversification results in CDRHs, 100% (130 CDRHs) of the CDRHs from RNL cloned R genes did not have an RNL domain. Diversification was also observed in CDRHs from cloned R genes that were TN (62% or 8 out of 13 CDRHs), TNL (55% or 752 out of 1356 CDRHs), NL (51% or 121 out of 236 CDRHs), CNL (49% or 128 out of 332 CDRHs), LRR-RLP (5% or 29 out of 628 CDRHs) and LRR-RLK (2% or 3 out of 170 CDRHs). Of the cloned R genes, which were NLs, all the CDRHs (29) had additional RGA domains, while for the LRR-RLP cloned R genes 59% (71 out of 121 diversified CDRHs) had an additional one or two RGA domains. On the other hand, the combination of truncation and addition of RGA domains was observed in CDRHs from cloned R genes TN (63% or 5 out 8 diversified CDRHs), TNL (55% or 411 out of 752 diversified CDRHs) and RNL (54% or 70 out of 130 diversified CDRHs).

2.4. Identification of CDRH Clusters in Arabis alpina, Camelina sativa and Cardamine hirsuta

The organisation of CDRHs with RGA domains across chromosomes of A. alpina, C. sativa and C. hirsuta was studied to investigate the gene clustering of CDRHs in Brassica crop relatives. We identified a total of 72 gene clusters, consisting of 62 homogeneous RGA clusters (38 NLR, 17 RLK and 7 RLP clusters) and 10 heterogeneous RGA clusters (Figure 4, Figure 5 and Figure 6). C. sativa contained the highest number of gene clusters with 28 (Figure 5), followed by C. hirsuta with 24 gene clusters (Figure 6) and A. alpina with 20 gene clusters (Figure 4).

3. Discussion

By aligning the 49 cloned R genes from 11 diseases, across 20 Brassicaceae genomes (crop species C. sativa, R. sativus and S. alba and wild species A. halleri, A. lyrata, A. alpina, B. vulgaris, B. stricta, B. cretica, C. grandiflora, C. bursa-pastoris, C. rubella, C. hirsuta, E. salsugineum, L. alabamica, L. meyenii, R. raphanistrum, Sisymbrium irio, S. parvula and T. arvense), an inventory of specific RGAs associated with cloned R genes was found. This provides an opportunity to search for novel CDRHs, which may confer disease resistance (especially the CDRHs in wild species), which can be used for future crop improvement once function is established in the crop species. Once cloned, molecular markers can be developed as a diagnostic tool in screening additional germplasm to characterise further lines for resistance.
The RGAs in B. cretica, C. bursa-pastoris and S. alba genomes and specific RGAs (CDRHs) obtained here are additional gene resources to the previously identified Brassicaceae RGA repertoire [51,56,57]. The number of S. alba RGAs in this study was higher than the RGAs obtained in the 18 species: Aethionema arabicum, A. halleri, A. lyrata, A. thaliana, A. alpina, B. vulgaris, B. stricta, B. rapa, C. grandiflora, C. rubella, C. hirsuta, E. salsugineum, L. alabamica, R. raphanistrum, R. sativus, S. irio, S. parvula and T. arvense genomes; the number of C. bursa-pastoris RGAs identified in this study was higher than the number of RGAs in the 21 species: Aethionema arabicum, A. halleri, A. lyrata, A. thaliana, A. alpina, B. vulgaris, B. stricta, B. rapa, B. nigra, B. oleracea, C. grandiflora, C. rubella, C. hirsuta, E. salsugineum, L. alabamica, R. raphanistrum, R. sativus, S. irio, S. parvula and T. arvense genomes [51,58]. Only the tetraploid Brassica crops (B. juncea, B. napus and B. carinata), C. sativa (hexaploid) and the wild species L. meyenii (octaploid) had greater numbers of RGAs than C. bursa-pastoris (tetraploid) [51,56], indicating that polyploidisation is a factor leading to more RGAs in species in the Brassicaceae family. Polyploid plants also have a greater number of transposable elements, an evolution driver of genome expansion [59,60], compared to its progenitors [61,62].
Brassica crops have experienced extensive breeding and development to improve disease resistance due to their long history of domestication that may have been a factor for RGA number expansion [63]. A previous study showed an average of 1563 RGAs in 11 genomes of the domesticated species compared to the average of 863 RGAs in 19 genomes of the wild species [51]; a similar trend was observed in this study between the domesticated and wild species. The number of RGAs in B. cretica (wild species) in this study was lower compared to the number of RGAs found in domesticated Brassica crops. This was also the case with the specific RGAs for R. sativus and R. raphanistrum (CDRHs in this study) and the RGAs obtained in a previous study [51], where domesticated radish had more RGAs compared to wild radish. However, this is not always the case as B. macrocarpa (wild cabbage species) had more RGAs compared to 10 domesticated cabbage species in pangenome analysis [58]. Here, the lesser RGAs in B. cretica and R. raphanistrum than their domesticated counterpart species may also be due to the quality of genomes, as domesticated crops often have better genome qualities.
The domesticated Brassicaceae members (used in this study) have also been reported as excellent sources of disease resistance. For instance, C. sativa has been reported to have R genes providing resistance against Alternaria black spot, blackleg, downey mildew and Sclerotinia stem rot [40,64,65], R. sativus has resistance against black rot [66], clubroot [67,68], downey mildew [69,70], Fusarium wilt [71], white rust [72] and Turnip mosaic virus [73,74] and S. alba has resistance to blackleg [39,75], Turnip mosaic virus [76] and Sclerotinia stem rot [77,78]. However, further investigation is needed as to whether the RGAs we identified in these three species are associated with the resistant phenotype. Nevertheless, our study supports the previous findings and the RGAs we identified are a valuable reference for future studies.
Unlike the cultivated crops, information towards genetic disease resistance in Brassicaceae wild species is limited. Of the wild Brassicaceae species we included, a few of them have been reported previously as potential R gene source against a particular disease, for instance, B. vulgaris against Alternaria black spot and black rot [79], B. cretica against Verticillium wilt disease [80], C. bursa-pastoris against clubroot [81], Sclerotinia stem rot [82] and Alternaria black spot [83], R. raphanistrum against blackleg [38], clubroot [84], downey mildew [85] and Sclerotinia stem rot [86] and T. arvense against blackleg [42]. However, the association between the reported phenotypic disease resistance in these species and the identified RGAs here needs further research.
The retention and diversification of RGA domains in the Brassicaceae family are a result of evolutionary events, such as whole-genome triplication/duplication [87,88,89,90,91]. Homologs may confer similar or dissimilar function to the reference gene [92,93]. A functional study revealed the A. lyrata homologs AL.MTP11A and AL.MTP11B are redundant to AT.MTP11 in A. thaliana [94], a gene involved in Mn2+ transport and tolerance [95]. Similarly, AL.TSO2A and AL.TSO2B in A. lyrata are homologous to AT.TSO2 in A. thaliana [94], a gene functionally related to ribonucleotide reductase [96]. On the other hand, diversification in domains may indicate a different function of the original gene. For instance, the At_RPP1 homolog At_RPP1Nd (Nd accession) recognises a single allele of Avr gene ATR1NdWsB, while At_RPP1WsB (WsB accession) also detects ATR1NdWsB plus three additional alleles with divergent sequences to confer resistance against downey mildew [97].
RGA domains have also been reported to be prone to alteration, such as truncation or even loss of function, as they respond to selection pressure (e.g., presence of virulent pathogens) [98,99]. Truncated R genes encoding two-part proteins, such as CN, TN and NL, are evolutionary gene reservoirs and they readily allow for the formation of new genes through duplications, translocation and fusions [100,101,102]. In an RGA, added LRR domains can indicate pathogen specificity. For instance, the LRR domain in At_RPP1 directly interacts with Avr ATR1 [103], much like the L6 recognition of AvrL567 and the L11 recognition of AvrL11 [104,105]. The LRR domain is also important for gene/protein stability [106]. Solo RGA domains could also confer resistance, as reports showed that the overexpression of NBS domains in a potato R gene Rx (CNL) resulted in an HR [107]. However, the case is different to the CC domain overexpression in At_RPS5, as it did not yield a hypersensitive response, but when both CC and NBS were overexpressed, it resulted in a hypersensitive response [108].
In gene clustering, C. sativa contained the highest total number of CDRHs clusters due to its higher number of chromosomes, 20, compared to 8 chromosomes of A. alpina and C. hirsuta. The RGA clusters are more prone to evolutionary processes, such as sequence exchanges, insertion or duplication, followed by neofunctionalisation [109,110,111,112]. The NLRs in a gene cluster can undergo mono or polymerisation, which results in massive expansions of pathogen recognition [111]. For instance, an NLR cluster with eight members contained two functionally characterised R genes, At_RPP4 and At_RPP5, recognizing the Avr genes ATR4 and ATR5 in the downey mildew resistance response, respectively [113]. Furthermore, it has been shown that RLPs in a gene cluster are most likely pathogen responsive [114]. Two cloned RLP genes, At_RLP30 and At_RLP32, which are involved in bacterial leaf spot resistance, form a gene cluster on At03 in A. thaliana [56,115,116], while a gene cluster on A10 in B. napus consists of LepR3/Rlm2, two alleles of a cloned RLP gene that confers blackleg resistance [117,118] and a homolog of At_PBS1 [56]. On the other hand, 16 RLK clusters associated with disease resistance were found in A. thaliana and Brassica crops [56]. Heterogeneous gene clusters with members having RGA domains and including secreted peptides associated to blackleg and clubroot were also observed in B. napus [119]. Thus, the CDRHs obtained here, especially those that were clustered, are putative R genes that may confer disease resistance.

4. Materials and Methods

4.1. Mining the Protein Sequences of the Cloned Genes

In total, 49 cloned R genes identified in Brassica crop species and A. thaliana that confer resistance against fungal and bacterial diseases that affect Brassicaceae species (Table 2) were selected based on the following criteria set in a previous study [56]: (1) the R gene pairs to an effector or Avr gene in a gene-for-gene resistance or (2) confers resistance in the form of a hypersensitive response (usually observed early stage), indicating its involvement in a gene-for-gene interaction or (3) acts as a helper or accessory gene pairing to the existing R–Avr interaction. The protein sequences of the 49 cloned R genes were retrieved from the UniProtKb (https://www.uniprot.org/uniprot/, verified and accessed on 8 August 2022) [120] or NCBI (https://www.ncbi.nlm.nih.gov/, verified and accessed on 8 August 2022) website.

4.2. Mining of Resistance Gene Analogs

The list of predicted RGAs and their subclasses (CN, CNL, NBS, NL, TNL, TX, CNL, TN, Other-NLR, Other-RLK, LRR-RLK, Lysm-RLK, LRR-RLP and Lysm-RLP) derived from the RGAugury pipeline [174] in A. alpina, A. halleri, A. lyrata, B. vulgaris, B. stricta, C. sativa, C. grandiflora, C. rubella, C. hirsuta, E. salsugineum, L. alabamica, L. meyenii, R. raphanistrum, R. sativus, S. irio, S. parvula and T. arvense genomes were taken from a previous study [51], available at https://research-repository.uwa.edu.au/en/datasets/brassicaceae-rga-candidate-protein-sequences, accessed on 23 November 2020. The RGAugury pipeline was also used in this study to perform in silico prediction of RGAs and their subclasses in the genomes of B. cretica [175], C. bursa-pastoris [176] and S. alba [177].

4.3. Identification of Homologs

The RGAs from the 20 Brassicaceae genomes and the 49 cloned R genes were aligned using Protein Basic Local Alignment Search Tool (BLASTp) [178]. From the BLASTp results, the criteria of the previous studies in identifying homologous genes in plants were applied by removing hits with greater than E-45 [56,179,180,181] and less than 148 amino acid or aa (coverage) [56] from further analyses. We applied an additional criterion by removing any BLASTp results lower than 60% similarity from further analyses as the homology search was conducted between crop R genes and several wild species. Further classification of RGAs was undertaken, according to whether they had the similar resistance domain to their homologous cloned R gene counterpart or whether it was different [56].

4.4. Gene Cluster Analysis

Among the 20 Brassicaceae species used in this study, only three genomes, A. alpina [182], C. hirsuta [11] and C. sativa [183], were used for gene cluster analysis, due to the accessibility of their pseudo-chromosomes (assigned chromosomes), from which gene clusters were derived. Two types of gene clusters were then identified, with the first defined as a homogenous RGA cluster (having at least 2–8 RGAs of the same class either NLR, RLK or RLP) situated within a 200 kb region on the same chromosome [184,185]. The second was defined as a heterogeneous cluster, containing different classes of RGAs [184,185].

5. Conclusions

CWRs with exotic genetic libraries provide rare RGAs, which could be a GMO alternative in improving disease resistance in Brassicaceae crops. This study suggests several domesticated and wild species could be a potential R gene source for a particular disease resistance. Based on their CDRHs having RGA domains, A. alpina and B. stricta, C. hirsuta and C. bursa-pastoris and C. sativa are good sources of resistance against white rust, black rot and Sclerotinia stem rot, respectively. Though the challenge remains in the gene transfer, several methodologies, such as bridging crosses, chromosome doubling after hybrid crossing and somatic hybridization, have found success in Brassicaceae crop breeding. Several CDRHs have also been found in less-explored disease resistance, such as Alternaria black spot, bacterial leaf spot, black rot, grey mould and powdery mildew in Brassicaceae crops, and the RGAs obtained are a valuable starting reference for future studies. Lastly, the current findings of CDRHs in crops C. sativa, R. sativus and S. alba and the 17 wild Brassicaceae species and the previous findings of CDRHs in A. thaliana and Brassica crops [56] provide an opportunity to study the evolutionary differences in 49 cloned R genes (reference in this study) and their homologs throughout the Brassicaceae family.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants11223010/s1, Table S1: List of resistance-gene analogs (RGAs) in Brassica cretica, Capsella bursa-pastoris and Sinapis alba using RGAugury pipeline. Table S2: List of resistance-gene analogs (RGAs) homologous to cloned disease resistance genes (R genes) and the E-value and similarity basis.

Author Contributions

A.Y.C. and J.B. conceptualized the paper; A.Y.C. wrote the original draft along with formal analyses; W.J.W.T. helped improve the paper by suggesting additional ideas and by thorough revision/editing; P.E.B. analysed the Brassica cretica, Capsella bursa-pastoris and Sinapis alba genes using the RGAugury pipeline; D.E. and J.B. supervised, reviewed and suggested revisions to the paper. All authors have read and agreed to the published version of the manuscript.

Funding

This study is funded by the Australian Research Council projects (DP200100762 and DP210100296) and Grains Research and Development Corporation UWA1905-006RTX.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data used in this research are publicly available. The protein sequences of each cloned gene can be found at https://www.uniprot.org/uniprot/ (accessed on 10 October 2020) and https://www.ncbi.nlm.nih.gov/ (accessed on 10 October 2020). The data (results) presented in this research are available in the Supplementary Materials.

Acknowledgments

All authors acknowledge the University of Western Australia Research Training Program economic support during A.Y.C. and W.J.W.T. respective doctoral studies. W.J.W.T. would also like to acknowledge the support of the Grains Research and Development Corporation.

Conflicts of Interest

The authors declare no known competing financial interests or personal relationships that could have influenced the work reported here.

References

  1. Al-Shehbaz, I.A. The Genera of Brassiceae (Cruciferae; Brassicaceae) in the Southeastern United States. J. Arnold Arbor. 1985, 66, 279–351. [Google Scholar] [CrossRef]
  2. Tamokou, J.D.D.; Mbaveng, A.T.; Kuete, V. Chapter 8-Antimicrobial Activities of African Medicinal Spices and Vegetables. In Medicinal Spices and Vegetables from Africa; Kuete, V., Ed.; Academic Press: Cambridge, MA, USA, 2017; pp. 207–237. [Google Scholar]
  3. Warwick, S.I.; Mummenhoff, K.; Sauder, C.A.; Koch, M.A.; Al-Shehbaz, I.A. Closing the gaps: Phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region. Plant Syst. Evol. 2010, 285, 209–232. [Google Scholar] [CrossRef]
  4. Koornneef, M.; Meinke, D. The development of Arabidopsis as a model plant. Plant J. 2010, 61, 909–921. [Google Scholar] [CrossRef] [PubMed]
  5. Palmer, C.E.; Warwick, S.; Keller, W. Brassicaceae (Cruciferae) family, plant biotechnology, and phytoremediation. Int. J. Phytoremed. 2001, 3, 245–287. [Google Scholar] [CrossRef]
  6. Wötzel, S.; Andrello, M.; Albani, M.C.; Koch, M.A.; Coupland, G.; Gugerli, F. Arabis alpina: A perennial model plant for ecological genomics and life-history evolution. Mol. Ecol. Resour. 2022, 22, 468–486. [Google Scholar] [CrossRef]
  7. Nielsen, N.J.; Nielsen, J.; Staerk, D. New resistance-correlated saponins from the insect-resistant crucifer Barbarea vulgaris. J. Agric. Food Chem. 2010, 58, 5509–5514. [Google Scholar] [CrossRef]
  8. Brukhin, V.; Osadtchiy, J.V.; Florez-Rueda, A.M.; Smetanin, D.; Bakin, E.; Nobre, M.S.; Grossniklaus, U. The Boechera Genus as a Resource for Apomixis Research. Front. Plant Sci. 2019, 10, 00392. [Google Scholar] [CrossRef] [Green Version]
  9. Nagaharu, U. Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn. J. Bot. 1935, 7, 389–452. [Google Scholar]
  10. Bansal, S.; Durrett, T.P. Camelina sativa: An ideal platform for the metabolic engineering and field production of industrial lipids. Biochimie 2016, 120, 9–16. [Google Scholar] [CrossRef] [Green Version]
  11. Gan, X.; Hay, A.; Kwantes, M.; Haberer, G.; Hallab, A.; Ioio, R.D.; Hofhuis, H.; Pieper, B.; Cartolano, M.; Neumann, U. The Cardamine hirsuta genome offers insight into the evolution of morphological diversity. Nat. Plants 2016, 2, 16167. [Google Scholar] [CrossRef] [Green Version]
  12. Wu, H.J.; Zhang, Z.; Wang, J.Y.; Oh, D.-H.; Dassanayake, M.; Liu, B.; Huang, Q.; Sun, H.X.; Xia, R.; Wu, Y. Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc. Natl. Acad. Sci. USA 2012, 109, 12219–12224. [Google Scholar] [CrossRef] [PubMed]
  13. Lee, J.Y.; Mummenhoff, K.; Bowman, J.L. Allopolyploidization and evolution of species with reduced floral structures in Lepidium L. (Brassicaceae). Proc. Natl. Acad. Sci. USA 2002, 99, 16835–16840. [Google Scholar] [CrossRef] [Green Version]
  14. Moser, B.R.; Evangelista, R.L.; Jham, G. Fuel properties of Brassica juncea oil methyl esters blended with ultra-low sulfur diesel fuel. Renew. Energy 2015, 78, 82–88. [Google Scholar] [CrossRef]
  15. Wilkes, M.A.; Takei, I.; Caldwell, R.A.; Trethowan, R.M. The effect of genotype and environment on biodiesel quality prepared from Indian mustard (Brassica juncea) grown in Australia. Ind. Crops Prod. 2013, 48, 124–132. [Google Scholar] [CrossRef]
  16. Rahman, M.; Khatun, A.; Liu, L.; Barkla, B.J. Brassicaceae Mustards: Traditional and Agronomic Uses in Australia and New Zealand. Molecules 2018, 23, 231. [Google Scholar] [CrossRef] [Green Version]
  17. Austin, D. Dye Plants and Dyeing, Revised edition: Daniel F. Austin, Book Review Editor. Econ. Bot. 2003, 57, 288. [Google Scholar] [CrossRef]
  18. Hamburger, M. Isatis tinctoria–From the rediscovery of an ancient medicinal plant towards a novel anti-inflammatory phytopharmaceutical. Phytochem. Rev. 2002, 1, 333. [Google Scholar] [CrossRef]
  19. Denisow, B. Flowering and pollen production of several f. brassicaceae ornamentals. J. Apic. Sci. 2008, 52, 13–21. [Google Scholar]
  20. Raza, A.; Hafeez, M.B.; Zahra, N.; Shaukat, K.; Umbreen, S.; Tabassum, J.; Charagh, S.; Khan, R.S.; Hasanuzzaman, M. The Plant Family Brassicaceae: Introduction, Biology, And Importance. In The Plant Family Brassicaceae; Hasanuzzaman, M., Ed.; Springer: Singapore, 2020; pp. 1–43. [Google Scholar]
  21. Barbetti, M.J.; Li, C.X.; Banga, S.S.; Banga, S.K.; Singh, D.; Sandhu, P.S.; Singh, R.; Liu, S.Y.; You, M.P. New host resistances in Brassica napus and Brassica juncea from Australia, China and India: Key to managing Sclerotinia stem rot (Sclerotinia sclerotiorum) without fungicides. Crop Prot. 2015, 78, 127–130. [Google Scholar] [CrossRef]
  22. Barbetti, M.J.; Li, C.X.; You, M.P.; Singh, D.; Agnihotri, A.; Banga, S.K.; Sandhu, P.S.; Singh, R.; Banga, S.S. Valuable New Leaf or Inflorescence Resistances Ensure Improved Management of White Rust (Albugo candida) in Mustard (Brassica juncea) Crops. J. Phytopathol. 2016, 164, 404–411. [Google Scholar] [CrossRef]
  23. Bhattacharya, I.; Dutta, S.; Mondal, S.; Mondal, B. Clubroot disease on Brassica crops in India. Can. J. Plant Pathol. 2014, 36, 154–160. [Google Scholar] [CrossRef]
  24. Chattopadhyay, C.; Kolte, S.J.; Waliyar, F. Diseases of Edible Oilseed Crops; CRC Press Inc.: Boca Raton, FL, USA, 2015. [Google Scholar]
  25. Mani, A.; Dutta, P.; Chatterjee, S. Diseases in Brassica vegetable crops and their Integrated Disease Management (IDM). Agric. Food E-Newsl. 2020, 2, 532–542. [Google Scholar]
  26. Li, C.X.; Sivasithamparam, K.; Walton, G.; Salisbury, P.; Burton, W.; Banga, S.S.; Banga, S.; Chattopadhyay, C.; Kumar, A.; Singh, R.; et al. Expression and relationships of resistance to white rust (Albugo candida) at cotyledonary, seedling, and flowering stages in Brassica juncea germplasm from Australia, China, and India. Aust. J. Agric. Res. 2007, 58, 259–264. [Google Scholar] [CrossRef]
  27. Balesdent, M.H.; Barbetti, M.J.; Li, H.; Sivasithamparam, K.; Gout, L.; Rouxel, T. Analysis of Leptosphaeria maculans Race Structure in a Worldwide Collection of Isolates. Phytopathology 2005, 95, 1061. [Google Scholar] [CrossRef] [Green Version]
  28. Marcroft, S.J.; Elliott, V.L.; Cozijnsen, A.J.; Salisbury, P.A.; Howlett, B.J.; Van de Wouw, A.P. Identifying resistance genes to in Australian cultivars based on reactions to isolates with known avirulence genotypes. Crop Pasture Sci. 2012, 63, 338–350. [Google Scholar] [CrossRef]
  29. Jo, S.J.; Jang, K.S.; Choi, Y.H.; Kim, J.C.; Choi, G.J. Development of convenient screening method for resistant radish to Plasmodiophora brassicae. Res. Plant Dis. 2011, 17, 161–168. [Google Scholar] [CrossRef] [Green Version]
  30. Fredua-Agyeman, R.; Jiang, J.; Hwang, S.-F.; Strelkov, S.E. QTL Mapping and Inheritance of Clubroot Resistance Genes Derived From Brassica rapa subsp. rapifera (ECD 02) Reveals Resistance Loci and Distorted Segregation Ratios in Two F2 Populations of Different Crosses. Front. Plant Sci. 2020, 11, 00899. [Google Scholar]
  31. Gan, C.; Yan, C.; Pang, W.; Cui, L.; Fu, P.; Yu, X.; Qiu, Z.; Zhu, M.; Piao, Z.; Deng, X. Identification of Novel Locus RsCr6 Related to Clubroot Resistance in Radish (Raphanus sativus L.). Front. Plant Sci. 2022, 13, 866211. [Google Scholar] [CrossRef]
  32. Liu, Y.; Xu, A.; Liang, F.; Yao, X.; Wang, Y.; Liu, X.; Zhang, Y.; Dalelhan, J.; Zhang, B.; Qin, M.; et al. Screening of clubroot-resistant varieties and transfer of clubroot resistance genes to Brassica napus using distant hybridization. Breed Sci. 2018, 68, 258–267. [Google Scholar] [CrossRef] [Green Version]
  33. Atri, C.; Akhatar, J.; Gupta, M.; Gupta, N.; Goyal, A.; Rana, K.; Kaur, R.; Mittal, M.; Sharma, A.; Singh, M.P.; et al. Molecular and genetic analysis of defensive responses of Brassica juncea-B. fruticulosa introgression lines to Sclerotinia infection. Sci. Rep. 2019, 9, 17089. [Google Scholar] [CrossRef] [Green Version]
  34. Rana, K.; Atri, C.; Akhatar, J.; Kaur, R.; Goyal, A.; Singh, M.P.; Kumar, N.; Sharma, A.; Sandhu, P.S.; Kaur, G.; et al. Detection of First Marker Trait Associations for Resistance Against Sclerotinia sclerotiorum in Brassica juncea–Erucastrum cardaminoides Introgression Lines. Front. Plant Sci. 2019, 10, 1015. [Google Scholar] [CrossRef] [Green Version]
  35. Kumari, P.; Singh, K.P.; Bisht, D.; Kumar, S. Somatic hybrids of Sinapis alba + Brassica juncea: Study of backcross progenies for morphological variations, chromosome constitution and reaction to Alternaria brassicae. Euphytica 2020, 216, 93. [Google Scholar] [CrossRef]
  36. Mei, J.; Shao, C.; Yang, R.; Feng, Y.; Gao, Y.; Ding, Y.; Li, J.; Qian, W. Introgression and pyramiding of genetic loci from wild Brassica oleracea into B. napus for improving Sclerotinia resistance of rapeseed. Theor. Appl. Genet. 2020, 133, 1313–1319. [Google Scholar] [CrossRef]
  37. Garg, H.; Banga, S.; Bansal, P.; Atri, C.; Banga, S.S. Hybridizing Brassica rapa with wild crucifers Diplotaxis erucoides and Brassica maurorum. Euphytica 2007, 156, 417–424. [Google Scholar] [CrossRef]
  38. Chen, C.Y.; Séguin-Swartz, G. Reaction of wild crucifers to Leptosphaeria maculans, the causal agent of blackleg of crucifers. Can. J. Plant Pathol. 1999, 21, 361–367. [Google Scholar] [CrossRef]
  39. Gugel, R.K.; Séguin-Swartz, G. Introgression of Blackleg Resistance from Sinapis alba into Brassica napus. In Proceedings of the Brassica 97: International Symposium on Brassicas: 10th Crucifer Genetics Workshop, Rennes, France, 23–27 September 1997; p. 222. [Google Scholar]
  40. Li, H.; Barbetti, M.J.; Sivasithamparam, K. Hazard from reliance on cruciferous hosts as sources of major gene-based resistance for managing blackleg (Leptosphaeria maculans) disease. Field Crops Res. 2005, 91, 185–198. [Google Scholar] [CrossRef]
  41. Mithen, R.F.; Magrath, R. Glucosinolates and Resistance to Leptosphaeria maculans in Wild and Cultivated Brassica Species. Plant Breed. 1992, 108, 60–68. [Google Scholar] [CrossRef]
  42. Pedras, M.S.; Chumala, P.B.; Suchy, M. Phytoalexins from Thlaspi arvense, a wild crucifer resistant to virulent Leptosphaeria maculans: Structures, syntheses and antifungal activity. Phytochemistry 2003, 64, 949–956. [Google Scholar] [CrossRef]
  43. Plümper, B. Somatische und Sexuelle Hybridisierung für den Transfer von Krankheitsresistenzen auf Brassica napus L. Ph.D. Thesis, Free University of Berlin, Berlin, Germany, 1995; p. 108. [Google Scholar]
  44. Tewari, J.P.; Bansal, V.K.; Tewari, I.; Gómez-Campo, C.; Stringam, G.R.; Thiagarajah, M.R. Reactions of some wild and cultivated accessions of Eruca against Leptosphaeria maculans. Cruciferae Newslett. 1996, 18, 130–131. [Google Scholar]
  45. Winter, H. Untersuchungen zur Introgression von Resistenzen gegen die Wurzelhals- und Stengelfäule [Leptosphaeria maculans (Desm.) Ces. et De Not.] aus Verwandten Arten in den Raps (Brassica napus L.). Ph.D. Thesis, Freie Universität Berlin Universitätsbibliothek, Berlin, Germany, 23 February 2004. [Google Scholar]
  46. Sekhwal, M.K.; Li, P.; Lam, I.; Wang, X.; Cloutier, S.; You, F.M. Disease Resistance Gene Analogs (RGAs) in Plants. Int. J. Mol. Sci. 2015, 16, 19248–19290. [Google Scholar] [CrossRef] [Green Version]
  47. Jones, J.D.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef] [Green Version]
  48. Le Roux, C.; Huet, G.; Jauneau, A.; Camborde, L.; Trémousaygue, D.; Kraut, A.; Zhou, B.; Levaillant, M.; Adachi, H.; Yoshioka, H.; et al. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 2015, 161, 1074–1088. [Google Scholar] [CrossRef] [Green Version]
  49. Ravensdale, M.; Bernoux, M.; Ve, T.; Kobe, B.; Thrall, P.H.; Ellis, J.G.; Dodds, P.N. Intramolecular Interaction Influences Binding of the Flax L5 and L6 Resistance Proteins to their AvrL567 Ligands. PLoS Pathog. 2012, 8, e1003004. [Google Scholar] [CrossRef]
  50. Whitham, S.; Dinesh-Kumar, S.P.; Choi, D.; Hehl, R.; Corr, C.; Baker, B. The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor. Cell 1994, 78, 1101–1115. [Google Scholar] [CrossRef]
  51. Tirnaz, S.; Bayer, P.; Inturrisi, F.; Zhang, F.; Yang, H.; Dolatabadian, A.; Neik, T.; Severn-Ellis, A.; Patel, D.; Ibrahim, M.; et al. Resistance gene analogs in the Brassicaceae: Identification, characterization, distribution and evolution. Plant Physiol. 2020, 184, 909–922. [Google Scholar] [CrossRef]
  52. Afzal, A.J.; Wood, A.J.; Lightfoot, D.A. Plant receptor-like serine threonine kinases: Roles in signaling and plant defense. Mol. Plant Microbe Interact. 2008, 21, 507–517. [Google Scholar] [CrossRef] [Green Version]
  53. Chisholm, S.T.; Coaker, G.; Day, B.; Staskawicz, B.J. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 2006, 124, 803–814. [Google Scholar] [CrossRef] [Green Version]
  54. Jeong, S.; Trotochaud, A.E.; Clark, S.E. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 1999, 11, 1925–1933. [Google Scholar] [CrossRef] [Green Version]
  55. Nadeau, J.A.; Sack, F.D. Control of stomatal distribution on the Arabidopsis leaf surface. Science 2002, 296, 1697–1700. [Google Scholar] [CrossRef]
  56. Cantila, A.Y.; Neik, T.X.; Tirnaz, S.; Thomas, W.J.W.; Bayer, P.E.; Edwards, D.; Batley, J. Mining of Cloned Disease Resistance Gene Homologs (CDRHs) in Brassica Species and Arabidopsis thaliana. Biology 2022, 11, 821. [Google Scholar] [CrossRef]
  57. Wu, P.; Shao, Z.Q.; Wu, X.Z.; Wang, Q.; Wang, B.; Chen, J.Q.; Hang, Y.Y.; Xue, J.Y. Loss retention and evolution of NBS-encoding genes upon whole genome triplication of Brassica rapa. Gene 2014, 540, 54–61. [Google Scholar] [CrossRef]
  58. Bayer, P.; Golicz, A.; Tirnaz, S.; Chan, C.K.K.; Edwards, D.; Batley, J. Variation in abundance of predicted resistance genes in the Brassica oleracea pangenome. Plant Biotechnol. J. 2019, 17, 789–800. [Google Scholar] [CrossRef] [Green Version]
  59. Fedoroff, N. Transposons and genome evolution in plants. Proc. Natl. Acad. Sci. USA 2000, 97, 7002. [Google Scholar] [CrossRef] [Green Version]
  60. Vicient, C.M.; Casacuberta, J.M. Impact of transposable elements on polyploid plant genomes. Ann. Bot. 2017, 120, 195–207. [Google Scholar] [CrossRef] [Green Version]
  61. Bayer, P.E.; Scheben, A.; Golicz, A.A.; Yuan, Y.; Faure, S.; Lee, H.; Chawla, H.S.; Anderson, R.; Bancroft, I.; Raman, H.; et al. Modelling of gene loss propensity in the pangenomes of three Brassica species suggests different mechanisms between polyploids and diploids. Plant Biotechnol. J. 2021, 19, 2488–2500. [Google Scholar] [CrossRef]
  62. Yaakov, B.; Meyer, K.; Ben-David, S.; Kashkush, K. Copy number variation of transposable elements in Triticum–Aegilops genus suggests evolutionary and revolutionary dynamics following allopolyploidization. Plant Cell Rep. 2013, 32, 1615–1624. [Google Scholar] [CrossRef]
  63. Dolatabadian, A.; Bayer, P.E.; Tirnaz, S.; Hurgobin, B.; Edwards, D.; Batley, J. Characterization of disease resistance genes in the Brassica napus pangenome reveals significant structural variation. Plant Biotechnol. J. 2020, 18, 969–982. [Google Scholar] [CrossRef] [Green Version]
  64. Jabeen, N. Agricultural, Economic and Societal Importance of Brassicaceae Plants. In The Plant Family Brassicaceae; Hasanuzzaman, M., Ed.; Springer: Singapore, 2020; pp. 45–128. [Google Scholar]
  65. Séguin-Swartz, G.; Gugel, R.K.; Strelkov, S.; Olivier, C.; Li, J.L.; Klein-Gebbinck, H.; Borhan, H.; Caldwell, C.; Falk, K.C. Diseases of Camelina sativa (false flax). Can. J. Plant Pathol. 2010, 31, 375–386. [Google Scholar] [CrossRef]
  66. Duan, Y.D.Y.; Wang, J.L.; Wang, H.P.; Zhang, X.; Shen, D.; Song, J.P.; Li, X. Genetic analysis on the resistance of different radish germplasm to black rot. J. Plant Genet. Resour. 2015, 16, 1–6. [Google Scholar]
  67. Zhan, Z.; Nwafor, C.C.; Hou, Z.; Gong, J.; Zhu, B.; Jiang, Y.; Zhou, Y.; Wu, J.; Piao, Z.; Tong, Y.; et al. Cytological and morphological analysis of hybrids between Brassicoraphanus, and Brassica napus for introgression of clubroot resistant trait into Brassica napus L. PLoS ONE 2017, 12, e0177470. [Google Scholar] [CrossRef]
  68. Yang, H.; Yuan, Y.; Wei, X.; Zhang, X.; Wang, H.; Song, J.; Li, X. A New Identification Method Reveals the Resistance of an Extensive-Source Radish Collection to Plasmodiophora brassicae Race 4. Agronomy 2021, 11, 792. [Google Scholar] [CrossRef]
  69. Coelho, P.; Valério, L.; Monteiro, A. Comparing Cotyledon, Leaf and Root Resistance To Downy Mildew in Radish (Raphanus sativus L). Euphytica 2022, 218, 84. [Google Scholar] [CrossRef]
  70. Xu, L.; Jiang, Q.W.; Wu, J.; Wang, Y.; Gong, Y.Q.; Wang, X.L.; Limera, C.; Liu, L.W. Identification and Molecular Mapping of the RsDmR Locus Conferring Resistance to Downy Mildew at Seedling Stage in Radish (Raphanus sativus L.). J. Integr. Agric. 2014, 13, 2362–2369. [Google Scholar] [CrossRef] [Green Version]
  71. Lee, O.N.; Koo, H.; Yu, J.W.; Park, H.Y. Genotyping-by-Sequencing-Based Genome-Wide Association Studies of Fusarium Wilt Resistance in Radishes (Raphanus sativus L.). Genes 2021, 12, 858. [Google Scholar] [CrossRef]
  72. Kolte, S.J.; Bordoloi, D.K.; Awasthi, R.P. The search for resistance to major diseases of rapeseed and mustard in India. In Proceedings of the GCIRC 8th International Rapeseed Congress, Saskatoon, SK, Canada, 9–11 July 1991; pp. 219–225. [Google Scholar]
  73. Nyalugwe, E.P.; Barbetti, M.J.; Jones, R.A. Studies on resistance phenotypes to Turnip mosaic virus in five species of Brassicaceae, and identification of a virus resistance gene in Brassica juncea. Eur. J. Plant Pathol. 2015, 141, 647–666. [Google Scholar] [CrossRef]
  74. Scholze, P.; Krämer, R.; Ryschka, U.; Klocke, E.; Schumann, G. Somatic hybrids of vegetable brassicas as source for new resistances to fungal and virus diseases. Euphytica 2010, 176, 1–14. [Google Scholar] [CrossRef]
  75. Khangura, R.; Aberra, M. Strains of Leptosphaeria maculans with the Capacity to Cause Crown Canker on Brassica carinata are Present in Western Australia. Plant Dis. 2006, 90, 832. [Google Scholar] [CrossRef]
  76. Mamula, D.; Juretic, N.; Horvath, J. Susceptibility of host plants to belladonna mottle and turnip yellow mosaic tymoviruses: Multiplication and distribution. Acta Phytopathol. Entomol. Hung. 1997, 32, 289–298. [Google Scholar]
  77. Kumari, P.; Singh, K.P. Characterization of Stable Somatic Hybrids of Sinapis alba and Brassica juncea for Alternaria blight, Sclerotinia sclerotiurum Resistance and Heat Tolerance. Indian Res. J. Ext. Educ. 2019, 19, 99–103. [Google Scholar]
  78. Li, A.; Wei, C.; Jiang, J.; Zhang, Y.; Snowdon, R.J.; Wang, Y. Phenotypic variation in progenies from somatic hybrids between Brassica napus and Sinapis alba. Euphytica 2009, 170, 289–296. [Google Scholar] [CrossRef] [Green Version]
  79. Westman, A.L.; Dickson, M. Disease reaction to Alternaria brassicicola and Xanthomonas campestris pv. campestris in Brassica nigra and other weedy crucifers. Crucif. Newslett. 1998, 20, 87–88. [Google Scholar]
  80. Happstadius, I.; Ljungberg, A.; Kristiansson, B.; Dixelius, C. Identification of Brassica oleracea germplasm with improved resistance to Verticillium wilt. Plant Breed. 2003, 122, 30–34. [Google Scholar] [CrossRef]
  81. Siemens, J. Interspecific Hybridisation between Wild Relatives and Brassica napus to Introduce New Resistance Traits into the Oilseed Rape Gene Pool. Czech J. Genet. Plant Breed. 2002, 38, 155–157. [Google Scholar] [CrossRef] [Green Version]
  82. Chen, H.F.; Wang, H.; Li, Z.Y. Production and genetic analysis of partial hybrids in intertribal crosses between Brassica species (B. rapa, B. napus) and Capsella bursa-pastoris. Plant Cell Rep. 2007, 26, 1791–1800. [Google Scholar] [CrossRef]
  83. Tewari, J.P. Current understanding of resistance to Alternaria brassicae in crucifers. In Rapeseeds in a Changing World, Proceedings of the 8th International Rapeseed Congress, Saskatoon, SK, Canada, 9 July 1991; McGregor, D., Ed.; Groupe Consultatif International de Recherche sur le Colza (GCIRC): Paris, France, 1991; pp. 471–476. [Google Scholar]
  84. Crute, I.; Gray, A.; Crisp, P.; Buczacki, S. Variation in Plasmodiophora brassicae and resistance to clubroot disease in brassicas and allied crops-a critical review. Plant Breed. Abstr. 1980, 50, 91–104. [Google Scholar]
  85. Mohammed, A.E.; You, M.P.; Al-lami, H.F.D.; Barbetti, M.J. Pathotypes and phylogenetic variation determine downy mildew epidemics in Brassica spp. in Australia. Plant Pathol. 2018, 67, 1514–1527. [Google Scholar] [CrossRef]
  86. Uloth, M.B.; You, M.P.; Finnegan, P.M.; Banga, S.S.; Banga, S.K.; Sandhu, P.S.; Yi, H.; Salisbury, P.A.; Barbetti, M.J. New sources of resistance to Sclerotinia sclerotiorum for crucifer crops. Field Crops Res. 2013, 154, 40–52. [Google Scholar] [CrossRef]
  87. Schmidt, R.; Bancroft, I. Genetics and Genomics of the Brassicaceae. Springer Science & Business Media: New York, NY, USA, 2010. [Google Scholar]
  88. Bowers, J.E.; Chapman, B.A.; Rong, J.; Paterson, A.H. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 2003, 422, 433–438. [Google Scholar] [CrossRef]
  89. Song, X.; Wei, Y.; Xiao, D.; Gong, K.; Sun, P.; Ren, Y.; Yuan, J.; Wu, T.; Yang, Q.; Li, X.; et al. Brassica carinata genome characterization clarifies U’s triangle model of evolution and polyploidy in Brassica. Plant Physiol. 2021, 186, 388–406. [Google Scholar] [CrossRef]
  90. Beilstein, M.A.; Nagalingum, N.S.; Clements, M.D.; Manchester, S.R.; Mathews, S. Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2010, 107, 18724. [Google Scholar] [CrossRef]
  91. Lysak, M.A.; Koch, M.A.; Pecinka, A.; Schubert, I. Chromosome triplication found across the tribe Brassiceae. Genome Res. 2005, 15, 516–525. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Wu, Q.; Han, T.-S.; Chen, X.; Chen, J.F.; Zou, Y.P.; Li, Z.W.; Xu, Y.C.; Guo, Y.L. Long-term balancing selection contributes to adaptation in Arabidopsis and its relatives. Genome Biol. 2017, 18, 217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Charlesworth, D. Balancing Selection and Its Effects on Sequences in Nearby Genome Regions. PLoS Genet. 2006, 2, e64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Das, M.; Haberer, G.; Panda, A.; Das Laha, S.; Ghosh, T.C.; Schäffner, A.R. Expression Pattern Similarities Support the Prediction of Orthologs Retaining Common Functions after Gene Duplication Events. Plant Physiol. 2016, 17, 2343. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  95. Gustin, J.L.; Zanis, M.J.; Salt, D.E. Salt, Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol. Biol. 2011, 11, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Wang, C.; Liu, Z. Arabidopsis ribonucleotide reductases are critical for cell cycle progression, DNA damage repair, and plant development. Plant Cell 2006, 18, 350–365. [Google Scholar] [CrossRef] [Green Version]
  97. Rehmany, A.P.; Gordon, A.; Rose, L.E.; Allen, R.L.; Armstrong, M.R.; Whisson, S.C.; Kamoun, S.; Tyler, B.M.; Birch, P.R.J.; Beynon, J.L. Differential Recognition of Highly Divergent Downy Mildew Avirulence Gene Alleles by RPP1 Resistance Genes from Two Arabidopsis Lines. Plant Cell 2005, 17, 1839–1850. [Google Scholar] [CrossRef] [Green Version]
  98. Faulkner, C.; Robatzek, S. Plants and pathogens: Putting infection strategies and defence mechanisms on the map. Curr. Opin. Plant Biol. 2012, 15, 699–707. [Google Scholar] [CrossRef]
  99. Nepal, M.P.; Benson, B.V. CNL disease resistance genes in soybean and their evolutionary divergence. Evol. Bioinform. 2015, 11, EBO.S21782. [Google Scholar] [CrossRef]
  100. Joshi, R.; Nayak, S. Perspectives of genomic diversification and molecular recombination towards R-gene evolution in plants. Physiol. Mol. Biol. Plants 2013, 19, 1–9. [Google Scholar] [CrossRef]
  101. Yue, J.X.; Meyers, B.C.; Chen, J.Q.; Tian, D.; Yang, S. Tracing the origin and evolutionary history of plant nucleotide-binding site–leucine-rich repeat NBS-LRR, genes. New Phytol. 2012, 193, 1049–1063. [Google Scholar] [CrossRef] [PubMed]
  102. Jacob, F.; Vernaldi, S.; Maekawa, T. Evolution and conservation of plant NLR functions. Front. Immunol. 2013, 4, 297–316. [Google Scholar] [CrossRef] [Green Version]
  103. Steinbrenner, A.D.; Goritschnig, S.; Staskawicz, B.J. Recognition and Activation Domains Contribute to Allele-Specific Responses of an Arabidopsis NLR Receptor to an Oomycete Effector Protein. PLoS Pathog. 2015, 11, e1004665. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  104. Ellis, J.; Dodds, P.; Pryor, T. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 2000, 3, 278–284. [Google Scholar] [CrossRef]
  105. Dodds, P.N.; Lawrence, G.J.; Catanzariti, A.-M.; Teh, T.; Wang, C.-I.; Ayliffe, M.A.; Kobe, B.; Ellis, J.G. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA 2006, 103, 8888–8893. [Google Scholar] [CrossRef] [Green Version]
  106. Zhang, Y.; Dorey, S.; Swiderski, M.; Jones, J.D. Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90. Plant J. 2004, 40, 213–224. [Google Scholar] [CrossRef]
  107. Rairdan, G.J.; Collier, S.M.; Sacco, M.A.; Baldwin, T.T.; Boettrich, T.; Moffett, P. The coiled-coil and nucleotide binding domains of the potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell 2008, 20, 739–751. [Google Scholar] [CrossRef] [Green Version]
  108. Ade, J.; DeYoung, B.J.; Golstein, C.; Innes, R.W. Indirect activation of a plant nucleotide binding site–leucine-rich repeat protein by a bacterial protease. Proc. Natl. Acad. Sci. USA 2007, 104, 2531–2536. [Google Scholar] [CrossRef] [Green Version]
  109. Michelmore, R.W.; Meyers, B.C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998, 8, 1113–1130. [Google Scholar] [CrossRef] [Green Version]
  110. Nützmann, H.-W.; Scazzocchio, C.; Osbourn, A. Metabolic gene clusters in eukaryotes. Annu. Rev. Genet. 2018, 52, 159–183. [Google Scholar] [CrossRef]
  111. van Wersch, S.; Li, X. Stronger When Together: Clustering of Plant NLR Disease resistance Genes. Trends Plant Sci. 2019, 24, 688–699. [Google Scholar] [CrossRef] [PubMed]
  112. Seah, S.; Telleen, A.C.; Williamson, V.M. Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues. Theor. Appl. Genet. 2007, 114, 1289–1302. [Google Scholar] [CrossRef] [PubMed]
  113. Meyers, B.; Kozik, A.; Griego, A.; Kuang, H.; Michelmore, R. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 2003, 15, 809–834. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  114. Steidele, C.E.; Stam, R. Multi-omics approach highlights differences between RLP classes in Arabidopsis thaliana. BMC Genom. 2021, 22, 557. [Google Scholar] [CrossRef] [PubMed]
  115. Wang, G.; Ellendorff, U.; Kemp, B.; Mansfield, J.W.; Forsyth, A.; Mitchell, K.; Bastas, K.; Liu, C.-M.; Woods-Tör, A.; Zipfel, C.; et al. A Genome-Wide Functional Investigation into the Roles of Receptor-Like Proteins in Arabidopsis. Plant Physiol. 2008, 147, 503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. Fan, L.; Fröhlich, K.; Melzer, E.; Albert, I.; Pruitt, R.N.; Zhang, L.; Albert, M.; Kim, S.-T.; Chae, E.; Weigel, D.; et al. Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1. Nat. Commun. 2022, 13, 1294. [Google Scholar] [CrossRef]
  117. Larkan, N.; Lydiate, D.; Yu, F.; Rimmer, S.; Borhan, H. Co-localisation of the blackleg resistance genes Rlm2 and LepR3 on Brassica napus chromosome A10. BMC Plant Biol. 2014, 14, 1595. [Google Scholar] [CrossRef] [Green Version]
  118. Larkan, N.J.; Ma, L.; Borhan, M.H. The Brassica napus receptor-like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus. Plant Biotechnol. J. 2015, 13, 983–992. [Google Scholar] [CrossRef]
  119. Stotz, H.U.; Harvey, P.J.; Haddadi, P.; Mashanova, A.; Kukol, A.; Larkan, N.J.; Borhan, M.H.; Fitt, B.D.L. Genomic evidence for genes encoding leucine-rich repeat receptors linked to resistance against the eukaryotic extra- and intracellular Brassica napus pathogens Leptosphaeria maculans and Plasmodiophora brassicae. PLoS ONE 2018, 13, e0198201. [Google Scholar]
  120. The UniProt. UniProt: The universal protein knowledgebase in 2021. Nucleic Acids Res. 2021, 49, D480–D489. [Google Scholar] [CrossRef]
  121. Grant, J.J.; Chini, A.; Basu, D.; Loake, G.J. Targeted Activation Tagging of the Arabidopsis NBS-LRR gene, ADR1, Conveys Resistance to Virulent Pathogens. Mol. Plant Microbe Interact. 2003, 16, 669–680. [Google Scholar] [CrossRef] [PubMed]
  122. Castel, B.; Ngou, P.M.; Cevik, V.; Redkar, A.; Kim, D.S.; Yang, Y.; Ding, P.; Jones, J.D.G. Diverse NLR immune receptors activate defence via the RPW8-NLR NRG1. New Phytol. 2019, 222, 966–980. [Google Scholar] [CrossRef] [PubMed]
  123. Saile, S.C.; Jacob, P.; Castel, B.; Jubic, L.M.; Salas-Gonzáles, I.; Bäcker, M.; Jones, J.D.G.; Dangl, J.L.; El Kasmi, F. Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions. PLoS Biol. 2020, 18, e3000783. [Google Scholar] [CrossRef] [PubMed]
  124. Gao, M.; Wang, X.; Wang, D.; Xu, F.; Ding, X.; Zhang, Z.; Bi, D.; Cheng, Y.T.; Chen, S.; Li, X.; et al. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 2009, 6, 34–44. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  125. Albert, I.; Böhm, H.; Albert, M.; Feiler, C.E.; Imkampe, J.; Wallmeroth, N.; Brancato, C.; Raaymakers, T.M.; Oome, S.; Zhang, H.; et al. An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity. Nat. Plants 2015, 1, 15140. [Google Scholar] [CrossRef]
  126. Zhang, W.; Fraiture, M.; Kolb, D.; Löffelhardt, B.; Desaki, Y.; Boutrot, F.F.G.; Tör, M.; Zipfel, C.; Gust, A.A.; Brunner, F. Arabidopsis RECEPTOR-LIKE PROTEIN30 and Receptor-Like Kinase SUPPRESSOR OF BIR1-1/EVERSHED Mediate Innate Immunity to Necrotrophic Fungi. Plant Cell 2013, 25, 4227–4241. [Google Scholar] [CrossRef] [Green Version]
  127. Bent, A.F.; Kunkel, B.N.; Dahlbeck, D.; Brown, K.L.; Schmidt, R.; Giraudat, J.; Leung, J.; Staskawicz, B.J. RPS2 of Arabidopsis thaliana: A leucine-rich repeat class of plant disease resistance genes. Science 1994, 265, 1856–1860. [Google Scholar] [CrossRef]
  128. Gassmann, W.; Hinsch, M.E.; Staskawicz, B.J. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J. 1999, 20, 265–277. [Google Scholar] [CrossRef]
  129. Deslandes, L.; Olivier, J.; Theulieres, F.; Hirsch, J.; Feng, D.X.; Bittner-Eddy, P.; Beynon, J.; Marco, Y. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl. Acad. Sci. USA 2002, 99, 2404–2409. [Google Scholar] [CrossRef] [Green Version]
  130. Tabata, S.; Kaneko, T.; Nakamura, Y.; Kotani, H.; Kato, T.; Asamizu, E.; Miyajima, N.; Sasamoto, S.; Kimura, T.; Hosouchi, T.; et al. Sequence and analysis of chromosome 5 of the plant Arabidopsis thaliana. Nature 2000, 408, 823–826. [Google Scholar]
  131. Gómez-Gómez, L.; Boller, T. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 2000, 5, 1003–1011. [Google Scholar] [CrossRef]
  132. Century, K.S.; Shapiro, A.D.; Repetti, P.P.; Dahlbeck, D.; Holub, E.; Staskawicz, B.J. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 1997, 278, 1963–1965. [Google Scholar] [CrossRef]
  133. Swiderski, M.R.; Innes, R.W. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J. 2001, 26, 101–112. [Google Scholar] [CrossRef] [PubMed]
  134. Grant, M.R.; Godiard, L.; Straube, E.; Ashfield, T.; Lewald, J.; Sattler, A.; Innes, R.W.; Dangl, J.L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 1995, 269, 843–846. [Google Scholar] [CrossRef]
  135. Tornero, P.; Chao, R.A.; Luthin, W.N.; Goff, S.A.; Dangl, J.L. Large-scale structure-function analysis of the Arabidopsis RPM1 disease resistance protein. Plant Cell 2002, 14, 435–450. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  136. Axtell, M.J.; Staskawicz, B.J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 2003, 112, 369–377. [Google Scholar] [CrossRef] [Green Version]
  137. Day, B.; Dahlbeck, D.; Staskawicz, B.J. NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 2006, 18, 2782–2791. [Google Scholar] [CrossRef] [Green Version]
  138. Liu, J.; Elmore, J.M.; Lin, Z.-J.D.; Coaker, G. A Receptor-like Cytoplasmic Kinase Phosphorylates the Host Target RIN4, Leading to the Activation of a Plant Innate Immune Receptor. Cell Host Microbe 2011, 9, 137–146. [Google Scholar] [CrossRef] [Green Version]
  139. Mackey, D.; Belkhadir, Y.; Alonso, J.M.; Ecker, J.R.; Dangl, J.L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 2003, 112, 379–389. [Google Scholar] [CrossRef] [Green Version]
  140. Mackey, D.; Holt, B.F.; Wiig, A.; Dangl, J.L. RIN4 Interacts with Pseudomonas syringae Type III Effector Molecules and Is Required for RPM1-Mediated Resistance in Arabidopsis. Cell 2002, 108, 743–754. [Google Scholar] [CrossRef] [Green Version]
  141. Warren, R.F.; Henk, A.; Mowery, P.; Holub, E.; Innes, R.W. A Mutation within the Leucine-Rich Repeat Domain of the Arabidopsis Disease Resistance Gene RPS5 Partially Suppresses Multiple Bacterial and Downy Mildew Resistance Genes. Plant Cell 1998, 10, 1439–1452. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  142. Sarris, P.F.; Duxbury, Z.; Huh, S.U.; Ma, Y.; Segonzac, C.; Sklenar, J.; Derbyshire, P.; Cevik, V.; Rallapalli, G.; Saucet, S.B.; et al. A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors. Cell 2015, 161, 1089–1100. [Google Scholar] [CrossRef]
  143. Diener, A.C.; Ausubel, F.M. RESISTANCE TO FUSARIUM OXYSPORUM 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 2005, 171, 305–321. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  144. Shen, Y.; Diener, A.C. Arabidopsis thaliana RESISTANCE TO FUSARIUM OXYSPORUM 2 Implicates Tyrosine-Sulfated Peptide Signaling in Susceptibility and Resistance to Root Infection. PLoS Genet. 2013, 9, e1003525. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  145. Cole, S.J.; Diener, A.C. Diversity in receptor-like kinase genes is a major determinant of quantitative resistance to Fusarium oxysporum f.sp. matthioli. New Phytol. 2013, 200, 172–184. [Google Scholar] [CrossRef]
  146. Staal, J.; Kaliff, M.; Bohman, S.; Dixelius, C. Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J. 2006, 46, 218–230. [Google Scholar] [CrossRef]
  147. Ma, L.; Djavaheri, M.; Wang, H.; Larkan, N.J.; Haddadi, P.; Beynon, E.; Gropp, G.; Borhan, M.H. Leptosphaeria maculans Effector Protein AvrLm1 Modulates Plant Immunity by Enhancing MAP Kinase 9 Phosphorylation. iScience 2018, 3, 177–191. [Google Scholar] [CrossRef] [Green Version]
  148. Larkan, N.J.; Lydiate, D.J.; Parkin, I.A.; Nelson, M.N.; Epp, D.J.; Cowling, W.A.; Rimmer, S.R.; Borhan, M.H. The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 2013, 197, 595–605. [Google Scholar] [CrossRef]
  149. Larkan, N.J.; Ma, L.; Haddadi, P.; Buchwaldt, M.; Parkin, I.A.P.; Djavaheri, M.; Borhan, M.H. The Brassica napus Wall-Associated Kinase-Like WAKL, gene Rlm9 provides race-specific blackleg resistance. Plant J. 2020, 104, 892–900. [Google Scholar] [CrossRef]
  150. Haddadi, P.; Larkan, N.J.; Van de Wouw, A.; Zhang, Y.; Neik, T.X.; Beynon, E.; Bayer, P.; Edwards, D.; Batley, J.; Borhan, M.H. Brassica napus genes Rlm4 and Rlm7, conferring resistance to Leptosphaeria maculans, are alleles of the Rlm9 wall-associated kinase-like resistance locus. Plant Biotechnol. J. 2022, 20, 1229–1231. [Google Scholar] [CrossRef]
  151. Staal, J.; Kaliff, M.; Dewaele, E.; Persson, M.; Dixelius, C. RLM3, a TIR domain encoding gene involved in broad-range immunity of Arabidopsis to necrotrophic fungal pathogens. Plant J. 2008, 55, 188–200. [Google Scholar] [CrossRef] [PubMed]
  152. Jehle, A.K.; Fürst, U.; Lipschis, M.; Albert, M.; Felix, G. Perception of the novel MAMP eMax from different Xanthomonas species requires the Arabidopsis receptor-like protein ReMAX and the receptor kinase SOBIR. Plant Signal Behav. 2013, 8, e27408. [Google Scholar] [CrossRef]
  153. Jehle, A.K.; Lipschis, M.; Albert, M.; Fallahzadeh-Mamaghani, V.; Fürst, U.; Mueller, K.; Felix, G. The Receptor-Like Protein ReMAX of Arabidopsis Detects the Microbe-Associated Molecular Pattern eMax from Xanthomonas. Plant Cell 2013, 25, 2330–2340. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  154. Albert, I.; Zhang, L.; Bemm, H.; Nürnberger, T. Structure-Function Analysis of Immune Receptor AtRLP23 with Its Ligand nlp20 and Coreceptors AtSOBIR1 and AtBAK1. Mol. Plant Microbe Interact. 2019, 32, 1038–1046. [Google Scholar] [CrossRef] [PubMed]
  155. Zhang, L.; Kars, I.; Essenstam, B.; Liebrand, T.W.H.; Wagemakers, L.; Elberse, J.; Tagkalaki, P.; Tjoitang, D.; van den Ackerveken, G.; van Kan, J.A.L. Fungal Endopolygalacturonases Are Recognized as Microbe-Associated Molecular Patterns by the Arabidopsis Receptor-Like Protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol. 2014, 164, 352–364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  156. Botella, M.A.; Parker, J.E.; Frost, L.N.; Bittner-Eddy, P.D.; Beynon, J.L.; Daniels, M.J.; Holub, E.B.; Jones, J.D.G. Three Genes of the Arabidopsis RPP1 Complex Resistance Locus Recognize Distinct Peronospora parasitica Avirulence Determinants. Plant Cell 1998, 10, 1847. [Google Scholar] [CrossRef] [Green Version]
  157. Sinapidou, E.; Williams, K.; Nott, L.; Bahkt, S.; Tör, M.; Crute, I.; Bittner-Eddy, P.; Beynon, J. Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant J. 2004, 38, 898–909. [Google Scholar] [CrossRef] [Green Version]
  158. van der Biezen, E.A.; Freddie, C.T.; Kahn, K.; Parker, J.E.; Jones, J.D. Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J. 2002, 29, 439–451. [Google Scholar] [CrossRef] [Green Version]
  159. Parker, J.E.; Coleman, M.J.; Szabò, V.; Frost, L.N.; Schmidt, R.; van der Biezen, E.A.; Moores, T.; Dean, C.; Daniels, M.J.; Jones, J.D. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 1997, 9, 879–894. [Google Scholar] [CrossRef] [Green Version]
  160. Barragan, C.A.; Wu, R.; Kim, S.-T.; Xi, W.; Habring, A.; Hagmann, J.; Van de Weyer, A.-L.; Zaidem, M.; Ho, W.W.H.; Wang, G.; et al. RPW8/HR repeats control NLR activation in Arabidopsis thaliana. PLoS Genet. 2019, 15, e1008313. [Google Scholar] [CrossRef]
  161. Tsuchiya, T.; Eulgem, T. An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication. Proc. Natl. Acad. Sci. USA 2013, 110, E3535–E3543. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  162. McDowell, J.M.; Dhandaydham, M.; Long, T.A.; Aarts, M.G.; Goff, S.; Holub, E.B.; Dangl, J.L. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 1998, 10, 1861–1874. [Google Scholar] [CrossRef] [PubMed]
  163. Bittner-Eddy, P.D.; Crute, I.R.; Holub, E.B.; Beynon, J.L. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 2000, 21, 177–188. [Google Scholar] [CrossRef] [PubMed]
  164. Goritschnig, S.; Krasileva, K.V.; Dahlbeck, D.; Staskawicz, B.J. Computational Prediction and Molecular Characterization of an Oomycete Effector and the Cognate Arabidopsis Resistance Gene. PLoS Genet. 2012, 8, e1002502. [Google Scholar] [CrossRef] [Green Version]
  165. Xiao, S.; Ellwood, S.; Calis, O.; Patrick, E.; Li, T.; Coleman, M.; Turner, J.G. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 2001, 291, 118–120. [Google Scholar] [CrossRef]
  166. Borhan, M.H.; Holub, E.B.; Beynon, J.L.; Rozwadowski, K.; Rimmer, S.R. The Arabidopsis TIR-NB-LRR gene RAC1 confers resistance to Albugo candida white rust, and is dependent on EDS1 but not PAD4. Mol. Plant Microbe Interact. 2004, 17, 711–719. [Google Scholar] [CrossRef] [Green Version]
  167. Borhan, M.H.; Gunn, N.; Cooper, A.; Gulden, S.; Tör, M.; Rimmer, S.R.; Holub, E.B. WRR4 encodes a TIR-NB-LRR protein that confers broad-spectrum white rust resistance in Arabidopsis thaliana to four physiological races of Albugo candida. Mol. Plant Microbe Interact. 2008, 21, 757–768. [Google Scholar] [CrossRef] [Green Version]
  168. Cevik, V.; Boutrot, F.; Apel, W.; Robert-Seilaniantz, A.; Furzer, O.J.; Redkar, A.; Castel, B.; Kover, P.X.; Prince, D.C.; Holub, E.B.; et al. Transgressive segregation reveals mechanisms of Arabidopsis immunity to Brassica-infecting races of white rust Albugo candida. Proc. Natl. Acad. Sci. USA 2019, 116, 2767–2773. [Google Scholar] [CrossRef] [Green Version]
  169. Arora, H.; Padmaja, K.L.; Paritosh, K.; Mukhi, N.; Tewari, A.K.; Mukhopadhyay, A.; Gupta, V.; Pradhan, A.K.; Pental, D. BjuWRR1, a CC-NB-LRR gene identified in Brassica juncea, confers resistance to white rust caused by Albugo candida. Theor. Appl. Genet. 2019, 132, 2223–2236. [Google Scholar] [CrossRef]
  170. Hatakeyama, K.; Niwa, T.; Kato, T.; Ohara, T.; Kakizaki, T.; Matsumoto, S. The tandem repeated organization of NB-LRR genes in the clubroot-resistant CRb locus in Brassica rapa L. Mol. Genet. Genom. 2017, 292, 397–405. [Google Scholar] [CrossRef]
  171. Ueno, H.; Matsumoto, E.; Aruga, D.; Kitagawa, S.; Matsumura, H.; Hayashida, N. Molecular characterization of the CRa gene conferring clubroot resistance in Brassica rapa. Plant Mol. Biol. 2012, 80, 621–629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  172. Hatakeyama, K.; Suwabe, K.; Tomita, R.N.; Kato, T.; Nunome, T.; Fukuoka, H.; Matsumoto, S. Identification and Characterization of Crr1a, a Gene for Resistance to Clubroot Disease Plasmodiophora brassicae Woronin, in Brassica rapa L. PLoS ONE 2013, 8, e54745. [Google Scholar] [CrossRef] [PubMed]
  173. Shimizu, M.; Pu, Z.J.; Kawanabe, T.; Kitashiba, H.; Matsumoto, S.; Ebe, Y.; Sano, M.; Funaki, T.; Fukai, E.; Fujimoto, R.; et al. Map-based cloning of a candidate gene conferring Fusarium yellows resistance in Brassica oleracea. Theor. Appl. Genet. 2015, 128, 119–130. [Google Scholar] [CrossRef] [PubMed]
  174. Li, P.; Quan, X.; Jia, G.; Xiao, J.; Cloutier, S.; You, F.M. RGAugury: A pipeline for genome-wide prediction of resistance gene analogs RGAs, in plants. BMC Genom. 2016, 17, 852. [Google Scholar] [CrossRef] [Green Version]
  175. Kioukis, A.; Michalopoulou, V.A.; Briers, L.; Pirintsos, S.; Studholme, D.J.; Pavlidis, P.; Sarris, P.F. Intraspecific diversification of the crop wild relative Brassica cretica Lam. using demographic model selection. BMC Genom. 2020, 21, 48. [Google Scholar] [CrossRef] [Green Version]
  176. Kasianov, A.S.; Klepikova, A.V.; Kulakovskiy, I.V.; Gerasimov, E.S.; Fedotova, A.V.; Besedina, E.G.; Kondrashov, A.S.; Logacheva, M.D.; Penin, A.A. High-quality genome assembly of Capsella bursa-pastoris reveals asymmetry of regulatory elements at early stages of polyploid genome evolution. Plant J. 2017, 91, 278–291. [Google Scholar] [CrossRef] [Green Version]
  177. Platts, A.; Shu, S.; Wright, S.; Barry, K.; Edger, P.; Pires, J.C.; Schmutz, J. WGS Assembly of Sinapis alba; DOE Joint Genome Institute: Berkeley, CA, USA, 2020.
  178. Altschul, S.F.; Madden, T.L.; Schäffer, A.A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 1997, 25, 3389–3402. [Google Scholar] [CrossRef] [Green Version]
  179. Rameneni, J.J.; Lee, Y.; Dhandapani, V.; Yu, X.; Choi, S.R.; Oh, M.-H.; Lim, Y.P. Genomic and Post-Translational Modification Analysis of Leucine-Rich-Repeat Receptor-Like Kinases in Brassica rapa. PLoS ONE 2015, 10, e0142255. [Google Scholar] [CrossRef]
  180. Wei, Z.; Wang, J.; Yang, S.; Song, Y. Identification and expression analysis of the LRR-RLK gene family in tomato Solanum lycopersicum, Heinz 1706. Genome 2015, 58, 121–134. [Google Scholar] [CrossRef]
  181. Yang, H.; Bayer, P.E.; Tirnaz, S.; Edwards, D.; Batley, J. Genome-Wide Identification and Evolution of Receptor-Like Kinases RLKs, and Receptor like Proteins RLPs in Brassica juncea. Biology 2021, 10, 17. [Google Scholar] [CrossRef]
  182. Willing, E.-M.; Rawat, V.; Mandáková, T.; Maumus, F.; James, G.V.; Nordström, K.J.; Becker, C.; Warthmann, N.; Chica, C.; Szarzynska, B. Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat. Plants 2015, 1, nplants201423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  183. Kagale, S.; Koh, C.; Nixon, J.; Bollina, V.; Clarke, W.E.; Tuteja, R.; Spillane, C.; Robinson, S.J.; Links, M.G.; Clarke, C. The emerging biofuel crop Camelina sativa retains a highly undifferentiated hexaploid genome structure. Nat. Commun. 2014, 5, 3706. [Google Scholar] [CrossRef] [PubMed]
  184. Holub, E.B. The arms race is ancient history in Arabidopsis, the wildflower. Nat. Rev. Genet. 2001, 2, 516–527. [Google Scholar] [CrossRef] [PubMed]
  185. Jupe, F.; Pritchard, L.; Etherington, G.J.; Mackenzie, K.; Cock, P.J.; Wright, F.; Sharma, S.K.; Bolser, D.; Bryan, G.J.; Jones, J.D.; et al. Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genom. 2012, 13, 75. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. The number and distribution of resistance-gene analog (RGA) subclass nucleotide-binding site (NBS), coiled-coil (CC)-NBS or CN, CN-leucine rich repeats (LRR) or CNL, NBS-LRR or NL, Toll/Interleukin-1 receptor (TIR)-NBS-LRR or TNL, TIR-NBS or TN, TIR with unknown domains or TX, NBS-LRR with other domains or Other-NLR, LRR- receptor like kinase (RLK) or LRR-RLK, Lysin motif (LsyM)-RLK or LysM-RLK, RLK with other receptor or Other-RLK, LRR- receptor-like protein (RLP) or LRR-RLP and LysM-RLP in Brassica cretica (Bcr), Capsella bursa-pastoris (Cbp) and Sinapis alba (Sal) genomes.
Figure 1. The number and distribution of resistance-gene analog (RGA) subclass nucleotide-binding site (NBS), coiled-coil (CC)-NBS or CN, CN-leucine rich repeats (LRR) or CNL, NBS-LRR or NL, Toll/Interleukin-1 receptor (TIR)-NBS-LRR or TNL, TIR-NBS or TN, TIR with unknown domains or TX, NBS-LRR with other domains or Other-NLR, LRR- receptor like kinase (RLK) or LRR-RLK, Lysin motif (LsyM)-RLK or LysM-RLK, RLK with other receptor or Other-RLK, LRR- receptor-like protein (RLP) or LRR-RLP and LysM-RLP in Brassica cretica (Bcr), Capsella bursa-pastoris (Cbp) and Sinapis alba (Sal) genomes.
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Plants 11 03010 g002 550
Figure 2. The number and distribution of cloned disease resistance gene homologs containing resistance domains including nucleotide-binding site (NBS), coiled-coil (CC)-NBS or CN, CN-leucine rich repeats (LRR) or CNL, NBS-LRR or NL, Toll/Interleukin-1 receptor (TIR)-NBS-LRR or TNL, TIR-NBS or TN, TIR with unknown domains or TX, NBS-LRR with other domains or Other-NLR, LRR- receptor like kinase (RLK) or LRR-RLK, Lysin motif (LsyM)-RLK or LysM-RLK, RLK with other receptor or Other-RLK, LRR- receptor like protein (RLP) or LRR-RLP and LysM-RLP in Arabidopsis halleri (Aha), Arabidopsis lyrata (Aly), Arabis alpina (Aal), Barbarea vulgaris (Bvu), Boechera stricta (Bst), Brassica cretica (Bcr), Camelina sativa (Csa), Capsella grandiflora (Cgr), Capsella bursa-pastoris (Cbp), Capsella rubella (Cru), Cardamine hirsuta (Chi), Eutrema salsugineum (Esa), Leavenworthia alabamica (Lal), Lepidium meyenii (Lme), Raphanus raphanistrum (Rra), Raphanus sativus (Rsa), Sinapis alba (Sal), Sisymbrium irio (Sir), Schrenkiella parvula (Spa) and Thlaspi arvense (Tar) genomes.
Figure 2. The number and distribution of cloned disease resistance gene homologs containing resistance domains including nucleotide-binding site (NBS), coiled-coil (CC)-NBS or CN, CN-leucine rich repeats (LRR) or CNL, NBS-LRR or NL, Toll/Interleukin-1 receptor (TIR)-NBS-LRR or TNL, TIR-NBS or TN, TIR with unknown domains or TX, NBS-LRR with other domains or Other-NLR, LRR- receptor like kinase (RLK) or LRR-RLK, Lysin motif (LsyM)-RLK or LysM-RLK, RLK with other receptor or Other-RLK, LRR- receptor like protein (RLP) or LRR-RLP and LysM-RLP in Arabidopsis halleri (Aha), Arabidopsis lyrata (Aly), Arabis alpina (Aal), Barbarea vulgaris (Bvu), Boechera stricta (Bst), Brassica cretica (Bcr), Camelina sativa (Csa), Capsella grandiflora (Cgr), Capsella bursa-pastoris (Cbp), Capsella rubella (Cru), Cardamine hirsuta (Chi), Eutrema salsugineum (Esa), Leavenworthia alabamica (Lal), Lepidium meyenii (Lme), Raphanus raphanistrum (Rra), Raphanus sativus (Rsa), Sinapis alba (Sal), Sisymbrium irio (Sir), Schrenkiella parvula (Spa) and Thlaspi arvense (Tar) genomes.
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Figure 3. The number and distribution of cloned disease resistance gene homologs associated to Alternaria black spot (ABS), blackleg (BL), black rot (BR), bacterial leaf spot (BLS), clubroot (CR), downey mildew (DM), Fusarium wilt (FW), grey mould (GM), powdery mildew (PM), Sclerotinia stem rot (SSR) and white rust (WR) resistance in Arabidopsis halleri (Aha), Arabidopsis lyrata (Aly), Arabis alpina (Aal), Barbarea vulgaris (Bvu), Boechera stricta (Bst), Brassica cretica (Bcr), Camelina sativa (Csa), Capsella grandiflora (Cgr), Capsella bursa-pastoris (Cbp), Capsella rubella (Cru), Cardamine hirsuta (Chi), Eutrema salsugineum (Esa), Leavenworthia alabamica (Lal), Lepidium meyenii (Lme), Raphanus raphanistrum (Rra), Raphanus sativus (Rsa), Sinapis alba (Sal), Sisymbrium irio (Sir), Schrenkiella parvula (Spa) and Thlaspi arvense (Tar) genomes.
Figure 3. The number and distribution of cloned disease resistance gene homologs associated to Alternaria black spot (ABS), blackleg (BL), black rot (BR), bacterial leaf spot (BLS), clubroot (CR), downey mildew (DM), Fusarium wilt (FW), grey mould (GM), powdery mildew (PM), Sclerotinia stem rot (SSR) and white rust (WR) resistance in Arabidopsis halleri (Aha), Arabidopsis lyrata (Aly), Arabis alpina (Aal), Barbarea vulgaris (Bvu), Boechera stricta (Bst), Brassica cretica (Bcr), Camelina sativa (Csa), Capsella grandiflora (Cgr), Capsella bursa-pastoris (Cbp), Capsella rubella (Cru), Cardamine hirsuta (Chi), Eutrema salsugineum (Esa), Leavenworthia alabamica (Lal), Lepidium meyenii (Lme), Raphanus raphanistrum (Rra), Raphanus sativus (Rsa), Sinapis alba (Sal), Sisymbrium irio (Sir), Schrenkiella parvula (Spa) and Thlaspi arvense (Tar) genomes.
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Plants 11 03010 g004 550
Figure 4. Distribution of cloned disease resistance gene homologs in Arabis alpina (1st inner layer in their corresponding position in A. alpina genome). The tracks in the circos plot, from outer to inner, show chromosome (Chr) number and types of gene cluster. GC_NLR = gene cluster (GC) with all nucleotide-binding site leucine rice repeats (NLR) members, GC_RLP = GC with all receptor-like proteins (RLP) members, GC_RLK = GC with all receptor-like kinase proteins (RLK) members, GC_H = GC with members are a mixture of NLR, RLK and/or RLP, Chr = chromosome and M = position in million base pairs.
Figure 4. Distribution of cloned disease resistance gene homologs in Arabis alpina (1st inner layer in their corresponding position in A. alpina genome). The tracks in the circos plot, from outer to inner, show chromosome (Chr) number and types of gene cluster. GC_NLR = gene cluster (GC) with all nucleotide-binding site leucine rice repeats (NLR) members, GC_RLP = GC with all receptor-like proteins (RLP) members, GC_RLK = GC with all receptor-like kinase proteins (RLK) members, GC_H = GC with members are a mixture of NLR, RLK and/or RLP, Chr = chromosome and M = position in million base pairs.
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Plants 11 03010 g005 550
Figure 5. Distribution of cloned disease resistance gene homologs in Camelina sativa (1st inner layer in their corresponding position in C. sativa genome). The tracks in the circos plot, from outer to inner, show chromosome (Chr) number and types of gene cluster. GC_NLR = gene cluster (GC) with all nucleotide-binding site leucine rice repeats (NLR) members, GC_RLP = GC with all receptor-like proteins (RLP) members, GC_RLK = GC with all receptor-like kinase proteins (RLK) members, GC_H = GC with members are a mixture of NLR, RLK and/or RLP, Chr = chromosome and M = position in million base pairs.
Figure 5. Distribution of cloned disease resistance gene homologs in Camelina sativa (1st inner layer in their corresponding position in C. sativa genome). The tracks in the circos plot, from outer to inner, show chromosome (Chr) number and types of gene cluster. GC_NLR = gene cluster (GC) with all nucleotide-binding site leucine rice repeats (NLR) members, GC_RLP = GC with all receptor-like proteins (RLP) members, GC_RLK = GC with all receptor-like kinase proteins (RLK) members, GC_H = GC with members are a mixture of NLR, RLK and/or RLP, Chr = chromosome and M = position in million base pairs.
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Plants 11 03010 g006 550
Figure 6. Distribution of cloned disease resistance gene homologs in Cardamine hirsuta (1st inner layer in their corresponding position in C. hirsuta genome). The tracks in the circos plot, from outer to inner, show chromosome (Chr) number and types of gene cluster. GC_NLR = gene cluster (GC) with all nucleotide-binding site leucine rice repeats (NLR) members, GC_RLP = GC with all receptor-like proteins (RLP) members, GC_RLK = GC with all receptor-like kinase proteins (RLK) members, GC_H = GC with members are a mixture of NLR, RLK and/or RLP, Chr = chromosome and M = position in million base pairs.
Figure 6. Distribution of cloned disease resistance gene homologs in Cardamine hirsuta (1st inner layer in their corresponding position in C. hirsuta genome). The tracks in the circos plot, from outer to inner, show chromosome (Chr) number and types of gene cluster. GC_NLR = gene cluster (GC) with all nucleotide-binding site leucine rice repeats (NLR) members, GC_RLP = GC with all receptor-like proteins (RLP) members, GC_RLK = GC with all receptor-like kinase proteins (RLK) members, GC_H = GC with members are a mixture of NLR, RLK and/or RLP, Chr = chromosome and M = position in million base pairs.
Plants 11 03010 g006
Table
Table 1. Cloned genes with resistance against Brassicaceae diseases and their corresponding homologs (similar by sequence identity) along the homolog types across the 20 studied genomes.
Table 1. Cloned genes with resistance against Brassicaceae diseases and their corresponding homologs (similar by sequence identity) along the homolog types across the 20 studied genomes.
Cloned Gene (RGA Subclass)Same RGA
Domain		Different RGA Domain
(Total)		Total
At_ADR1 (NL)33 NL5 CNL, 6 NBS, 1 TNL (12)45
At_BAK1 (LRR-RLK)117 LRR-RLK2 Other-RLK (2)119
At_FLS2 (LRR-RLK)24 LRR-RLK024
At_NDR1 (TM)000
At_NRG1a (RNL)031 CNL, 28 NL, 1 LRR-RLP, 3 CN, 3 NBS (66)66
At_NRG1b (RNL)031 CNL, 26 NL, 1 LRR-RLP, 3 CN, 3 NBS (64)64
At_PBS1 (Other-RLK)20 Other-RLK020
At_RAC1 (TNL)48 TNL10 NL, 3 NBS, 13 TN, 6 TX, 1 Other-NLR (33)81
At_RFO1 (Other-RLK)119 Other-RLK0119
At_RFO2 (LRR-RLP)31 LRR-RLP28 LRR-RLK (28)59
At_RFO3 (Other-RLK)50 Other-RLK050
At_RIN4 (CC)000
At_RLM1a (TNL)61 TNL5 NBS, 12 NL, 9 Other-NLR, 16 TN, 38 TX (80)141
At_RLM1b (TNL)81 TNL4 NBS, 23 NL, 8 Other-NLR, 16 TN, 31 TX, 1 LRR-RLP (83)164
At_RLM3 (TN)5 TN3 NL, 2 NBS, 1 Other-NLR, 7 TNL, 4 TX (17)22
At_RLP1 (LRR-RLP)36 LRR-RLP036
At_RLP23 (LRR-RLP)117 LRR-RLP0117
At_RLP30 (LRR-RLP)47 LRR-RLP047
At_RLP32 (LRR-RLP)159 LRR-RLP1 LRR-RLK (1)160
At_RLP42 (LRR-RLP)112 LRR-RLP0112
At_RPM1 (NL)14 NL1 LRR-RLP, 1 NBS (2)16
At_RPP1 (TNL)26 TNL1 CNL, 22 Other-NLR, 2 NBS, 6 NL, 15 TN, 30 TX (76)102
At_RPP13 (CNL)14 CNL4 NBS, 1 CN, 16 NL (21)35
At_RPP2a (TNL)56 TNL19 NL, 9 Other-NLR, 7 TN, 7 TX (42)98
At_RPP2b (TNL)20 TNL1 CNL, 2 NBS, 3 NL, 4 Other-NLR (10)30
At_RPP39 (CNL) 71 CNL11 CN, 3 NBS, 26 NL, 3 LRR-RLP (43)114
At_RPP4 (TNL)8 TNL3 NL, 2 Other-NLR, 5 TN, 5 TX (15)23
At_RPP5 (TNL)8 TNL2 NL, 3 Other-NLR, 6 TN, 11 TX (22)30
At_RPP7 (NL)56 NL1 CN, 12 CNL, 1 LRR-RLP, 10 NBS (24)80
At_RPP8 (CNL)80 CNL12 CN, 6 NBS, 24 NL (42)122
At_RPS2 (NL)6 NL18 CNL, 3 NBS (21)27
At_RPS4 (TNL) 32 TNL1 NBS, 6 NL, 7 Other-NLR (14)46
At_RPS5 (TNL) 058 CNL, 6 CN, 7 NBS, 22 NL (93)93
At_Rpw8.1 (RNL)000
At_Rpw8.2 (RNL)000
At_RRS1 (TNL)26 TNL0 (15)41
At_SOBIR1 (LRR-RLK)26 LRR-RLK1 Other-RLK (1)27
At_WRR12 (TNL)29 TNL5 NL, 2 TX, 4 LRR-RLP (11)40
At_WRR4a (TNL)37 TNL4 NL, 4 Other-NLR, 6 TN, 33 TX (47)84
At_WRR4b (TNL) 51 TNL2 LRR-RLP, 5 NL, 6 Other-NLR, 17 TN, 38 TX (68)119
At_WRR8 (TNL)56 TNL12 TN, 4 NBS, 11 NL, 2 Other-NLR, 6 TX (35)91
At_WRR9 (NL)6 NL1 NBS, 1 Other-NLR, 9 TN, 35 TNL, 16 TX (62)68
Bju_WRR1 (CNL)39 CNL10 NL, 9 CN, 3 NBS (22)61
Bna_LepR3/Rlm2 (LRR-RLP)97 LRR-RLP097
Bna_MAPk (Other-RLK)8 Other-RLK08
Bna_Rlm9/4/7 (Other-RLK)101 Other-RLK0101
Bol_FocBo1 (TNL)23 TNL3 Other-NLR, 7 TN, 14 TX, 8 NL (32)55
Bra_cRa/cRb (TNL)14 TNL1 Other-NLR, 5 TN, 1NBS, 7 TX (14)28
Bra_Crr1a (TNL)28 TNL7 NL, 6 Other-NLR, 28 TN, 19 TX, 2 NBS (62)90
Total199211813172
At = Arabidopsis thaliana, Bju = Brassica juncea, Bol = Brassica oleracea, Bra = Brassica rapa, Bna = Brassica napus, Resistance-gene analogs (RGA) domain in comparison to the cloned gene. CN = coiled-coil (CC)-nucleotide-binding site (NBS), CNL = CC-NBS-leucine rice repeats (LRR), NL = NBS-LRR, TN = Toll/Interleukin-1 receptor (TIR)-LRR, TNL = Toll/Interleukin-1 receptor (TIR)-NBS-LRR, TX = Toll/Interleukin-1 receptor (TIR) with other domains, Other-NLR = NBS-LRR with other domains, RNL = resistance to powdery mildew 8 (Rpw8)-NBS-LRR, LRR-RLK = LRR-receptor-like kinase proteins (RLK), Other-RLK= RLK with other domains, LRR-RLP = LRR-receptor-like proteins, TM = transmembrane.
Table
Table 2. The 49 cloned R genes from Arabidopsis thaliana (At), Brassica juncea (Bju), Brassica napus (Bna) and Brassica rapa (Bra) used for homology searches.
Table 2. The 49 cloned R genes from Arabidopsis thaliana (At), Brassica juncea (Bju), Brassica napus (Bna) and Brassica rapa (Bra) used for homology searches.
Gene (Accession ID/Reference)Pathogen
At_ADR1 (Q9FW44 U) [121,122,123]Hyaloperonospora arabidopsidis F, Erysiphe cichoracearum F and Pseudomonas syringae B
At_BAK1 (Q94F62 U) and At_SOBIR1 (Q9SKB2 U) [124,125] and At_RLP30 (Q9MA83 U) [115,126]P. syringae and Sclerotinia sclerotiorum F
At_RPS2 (Q42484 U) [127], At_RPS4 (Q9XGM3 U) [128] and At_RPS5 (O64973 U) [129], At_FLS2 (Q9FL28 U) [130,131], At_NDR1 (O48915 U) [132], At_PBS1 (Q9FE20 U) [133], At_RLP32 (Q9M9X0 U) [116], At_RPM1 (Q39214 U) [134,135], At_RIN4 (Q8GYN5 U) [136,137,138,139,140] and At_RRS1 (P0DKH5 U) [141,142]P. syringae
At_NGR1a (Q9FKZ1 U) and At_NGR1b (Q9FKZ0 U) [122,123]Albugo candidaF, H. arabidopsidis,
and P. syringae
At_RFO1 (Q8RY17 U) [143], At_RFO2 (Q9SHI4 U) [144] and At_RFO3 (Q9LW83 U) [145]Fusarium oxysporum matthioli F
At_RLM1a (F4I594 U) and At_RLM1b (Q9CAK1 U) [146], Bna_MPK9 (A0A078IFE9 U) [147], Bna_LepR3/Rlm2 (I7C3X3 U/A0A0B5L618 U) [118,148], Bna_Rlm9/4/7 (CDX67982.1 N) [149,150]Leptosphaeria maculans F
At_RLM3 (Q9FT77 U) [151]L. maculans, Botrytis cinerea F,
Alternaria brassicicola F and A. brassicae F
At_RLP1 (Q9LNV9 U) [152,153]Xanthomonas spp. B
At_RLP23 (O48849 U) [125,154]S. sclerotiorum
At_RLP42 (Q9LJS0 U) [155]B. cinerea and H. arabidopsidis
At_RPP1 (F4J339 U) [156], At_RPP2a (F4JT78 U) and At_RPP2b (F4JT80 U) [157], At_RPP4 (F4JNA9 U) [158], At_RPP5 (F4JNB7 U) [159], At_RPP7 (Q8W3K0 U) [160,161], At_RPP8 (Q8W4J9 U) [162], At_RPP13 (Q9M667 U) [163] and At_RPP39 (H9BPR9 U) [164]H. arabidopsidis
At_Rpw8.1 (Q9C5Z7 U) and At_Rpw8.2 (Q9C5Z6 U) [165]E. cichoracearum
At_RAC1 (Q6QX58 U) [166], At_WRR4a (Q9C7X0 U) and At_WRR4b (MK034466 N) [167], At_WRR8 (MK034463 N), At_WRR9 (MK034464 N), At_WRR12 (MK034462 N) [168] and Bju_WRR1 (A0A0B5L618 U) [169]A. candida
Bra_cRa/cRb (M5A8J3 U) [170,171] and Bra_Crr1a (AB605024.1 N) [172]Plasmodiophora brassicae F
Bol_FocBo1 (BAQ21734.1 N) [173]F. oxysporum f. sp. Conglutinans F
F = fungus, B = bacteria, RGA = resistance-gene analog, U = https://www.uniprot.org/uniprot/, accessed on 10 October 2020) website, N = https://www.ncbi.nlm.nih.gov/ (accessed on 10 October 2020).
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Cantila, A.Y.; Thomas, W.J.W.; Bayer, P.E.; Edwards, D.; Batley, J. Predicting Cloned Disease Resistance Gene Homologs (CDRHs) in Radish, Underutilised Oilseeds, and Wild Brassicaceae Species. Plants 2022, 11, 3010. https://doi.org/10.3390/plants11223010

AMA Style

Cantila AY, Thomas WJW, Bayer PE, Edwards D, Batley J. Predicting Cloned Disease Resistance Gene Homologs (CDRHs) in Radish, Underutilised Oilseeds, and Wild Brassicaceae Species. Plants. 2022; 11(22):3010. https://doi.org/10.3390/plants11223010

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Cantila, Aldrin Y., William J. W. Thomas, Philipp E. Bayer, David Edwards, and Jacqueline Batley. 2022. "Predicting Cloned Disease Resistance Gene Homologs (CDRHs) in Radish, Underutilised Oilseeds, and Wild Brassicaceae Species" Plants 11, no. 22: 3010. https://doi.org/10.3390/plants11223010

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