Abstract
Weeds are one of the main problems faced by agronomists, which are the cause of large losses of crops in many farmlands. Screening of novel biocontrol agents against weeds is highly desired to control a wide variety of weeds. The endophytic fungal isolate HL-1 was isolated from the phyllosphere of Cirsium setosum indigenous to agricultural fields of Hualong, Qinghai Province. The isolate was evaluated for its herbicidal activity against target weeds and its safety to major crops. The feasibility of solid substrate fermentation for the spore production of isolate HL-1 has been examined. The results indicated that the disease incidences of Galium aparine, Chenopodium album, Malva crispa, and Polygonum lapathifolium applied with HL-1 filtrate were 96.24%, 87.48%, 55.71%, and 65.48%, and the fresh weight reductions were 69.04%, 72.02%, 66.12%, and 58.03%, respectively. The filtrate was safe to Triticum aestivum and Vicia faba and slightly pathogenic to Brassica napus, Pisum sativum, and Hordeum vulgare. The strain was validated as Alternaria alternata by cultural characteristic and internal transcribed spacer sequencing. Optimization of the carbon and nitrogen sources for cultural media and materials for solid-state fermentation demonstrated that strain HL-1 had better colony growth and spore yield with the optimal carbon source of glucose, nitrogen source of yeast extract, and the optimal material was rapeseed cake. The optimal fermentation conditions of HL-1 are a temperature of 25 ℃, an inocula age of 72 h, initial moisture content of 40%, and an inoculated quantity of 8%. Its formulation showed a strong herbicidal activity on the tested weeds in both pot and field experiments, especially Stellaria media. Thus, phyllosphere microbiota is considered to be an important resource for implementing new biological herbicides for weed control, and this work provides a formulation of a mycoherbicide made up of spores produced by HL-1.
Similar content being viewed by others
References
Abbas HK, Boyette CD (2000) Solid substrate formulations of the mycoherbicide Colletotrichum truncatum for Hemp sesbania (Sesbania exaltata) control. Biocontrol Sci Techn 10:291–300
Arshad J, Sajjad A (2011a) Alternative management of a problematic weed of wheat Avena fatua L. by metabolites of Trichoderma. Chil J Agr Res 71:205–211
Arshad J, Sajjad A (2011b) Herbicidal activity of culture filtrates of Trichoderma sp. against two problematic weeds of wheat. Nat Prod Res 25:730–740
Ash GJ (2010) The science, art and business of successful bioherbicides. Biol Control 52:230–240
Avedi EK, Ochieno DMW, Ajanga S, Wanyama C, Wainwright H, Elzein A, Beed F (2014) Fusarium oxysporum f. sp. strigae strain Foxy 2 did not achieve biological control of Striga hermonthica parasitizing maize in Western Kenya. Biol Control 77:7–14
Babu RM, Sajeena A, Seetharaman K (2004) Solid substrate for production of Alternaria alternata conidia: a potential mycoherbicide for the control of Eichhornia crassipes (water hyacinth). Weed Res 44:298–304
Bailey KL, Boyetchko SM, Peng G et al (2009) Developing weed control technologies with fungi. In: Rai M (ed) Advances in fungal biotechnology. I.K. International Pub House, New Delhi, pp 1–44
Bastos BO, Deobald GA, Brun T, Dal-Prá V, Junges E, Kuhn RC, Pinto AK, Mazutti MA (2017) Solid-state fermentation for production of a bioherbicide from Diaporthe sp. and its formulation to enhance the efficacy. 3 Biotech 7:1–9
Berestetskiy A (2021) Development of mycoherbicides. Zaragoza O, Casadevall A(ed) Encyclopedia of Mycology, 1st edn. Elsevier, Netherlands, pp 629–640
Berestetskiy AO, Gasich EL, Poluektova EV, Nikolaeva EV, Sokornova SV, Khlopunova LB (2014) Biological activity of fungi from the phyllosphere of weeds and wild herbaceous plants. Microbiology 5:523–530
Berestetskiy AO, Panteleeva AS, Gannibal FB, Gomzhina MM, Gasich EL, Sokornova SV (2017) Physiological, biochemical properties and biological activity of Phoma-like fungi isolated from the phyllosphere of weeds and wild herbaceous plants. Mikol Fitopatol 5:283–291
Berestetskiy AO, Gannibal FB, Minkovich EV, Osterman IA, Salimova DR, Sergiev PV, Sokornova SV (2018) Spectrum of biological activity of the Alternaria fungi Isolated from the phyllosphere of herbaceous plants. Microbiology 87:806–816
Bhargav S, Panda BP, Ali M, Javed S (2008) Solid-state fermentation: an overview. Chem Biochem Eng Q 22:49–70
Boari A, Vurro M (2004) Evaluation of Fusarium spp. and other fungi as biological control agents of broomrape (Orobanche ramosa). Biol Control 30:212–219
Card S, Johnson L, Teasdale S, Caradus J (2016) Deciphering endophyte behaviour: the link between endophyte biology and efficacious biological control agents. FEMS Microbiol Ecol 92:1–19
Chauhan BS, Matloob A, Mahajan G, Aslam F, Florentine SK, Jha P (2017) Emerging challenges and opportunities for education and research in weed science. Front Plant Sci 8:1–13
Chen SG, Qiang S (2017) Recent advances in tenuazonic acid as a potential herbicide. Pestic Biochem Physiol 143:252–257
Choi GJ, Park JH, Kim HT, Lee SW, Kim JC (2004) Phytotoxicity of endophytic fungi and characterization of a phytotoxin isolated from Gliocladium catenulatum from Pinus densiflora. Kor J Mycol 32:8–15
Cordeau S, Triolet M, Wayman S, Steinberg C, Guillemin JP (2016) Bioherbicides: dead in the water? A review of the existing products for integrated weed management. Crop Prot 87:44–49
Dagno K, Lahlali R, Diourté M, Jijakli MH (2011a) Production and oil-emulsion formulation of Cadophora malorum and Alternaria jacinthicola, two biocontrol agents against water hyacinth (Eichhornia crassipes). Afr J Microbiol Res 5:924–929
Dagno K, Lahlali R, Diourté M, Jijakli MH (2011b) Effect of temperature and water activity on spore germination and mycelial growth of three fungal biocontrol agents against water hyacinth (Eichhornia crassipes). J Appl Microbiol 110:521–528
Dedjell A, Cliquet S (2019) Media and culturing protocol using a full 25 factorial design for the production of submerged aggregates by the potential bioherbicide Plectosporium alismatis against weed species of Alismataceae. Biocontrol Sci Techn 29:308–324
Deng W, Di YJ, Cai JX, Chen YY, Yuan SH (2018) Target-site resistance mechanisms to tribenuron-methyl and cross-resistance patterns to ALS-inhibiting herbicides of catchweed bedstraw (Galium aparine) with different ALS mutations. Weed Sci 67:183–188
Fang F, Zhang CX, Huang HJ, Li M, Gao XX, Li Y, Wei SH (2014) The occurrence of Tausch’s goatgrass (Aegilops tauschii Coss.) in wheat fields and its effect on wheat yield. Acta Ecol Sin 34:3917–3923
Firáková S, Šturdíková M, Múcková M (2007) Bioactive secondary metabolites produced by microorganisms associated with plants. Biologia 62:251–257
Gašić S, Tanović B (2013) Biopesticide formulations, possibility of application and future trends. Pesticidi i Phytomedicina 28:97–102
Gayathri S, Mythili S (2019) Fungal endophytes: a potent biocontrol agent and a bioactive metabolites reservoir. Biocatal Agric Biotechnol 21:101284
Grichar WJ (2008) Herbicide systems for control of horse purslane (Trianthema portulacastrum L.), smellmelon (Cucumis melo L.), and palmer amaranth (Amaranthus palmeri S. Wats) in peanut. Peanut Sci 35:38–42
Guo QY, Cheng L, Zhu HX, Li W, Wei YH, Chen HY, Guo LZ, Weng H, Wang J (2020) Herbicidal activity of Aureobasidium pullulans PA-2 on weeds and optimization of its solid-state fermentation conditions. J Integr Agric 19:173–182
Hoagland RE, Boyette CD, Abbas HK (2007) Myrothecium verrucaria isolates and formulations as bioherbicide agents for kudzu. Biocontrol Sci Techn 17:721–731
Hsieh CY, Tsai MJ, Hsu TH, Chang DM, Lo CT (2005) Medium optimization for polysaccharide production of Cordyceps sinensis. Appl Biochem Biotechnol 120:145–157
Júnior FWR, Scariot MA, Forte CT, Pandolfi L, Dil JM, Weirich S, Carezia C, Mulinari J, Mazutti MA, Fongaro G (2019) New perspectives for weeds control using autochthonous fungi with selective bioherbicide potential. Heliyon 5:e01676
Kim SW, Xu CP, Hwang HJ, Choi JW, Kim CW, Yun JW (2003) Production and characterization of exopolysaccharides from an enthomopathogenic fungus Cordyceps militaris NG3. Biotechnol Prog 19:428–435
Liu XC, Li HR, Kang T, Zhu ZY, Liu YL, Sun HQ, Pan LC (2019) The effect of fermentation conditions on the structure and anti-tumor activity of polysaccharides from Cordyceps gunnii. RSC Adv 9:18205–18216
Li XJ (2018) Main problems and management strategies of weeds in agricultural fields in China in recent years. Plant Prot 44:77–84
Mamy L, Gabrielle B, Barriuso E (2010) Comparative environmental impacts of glyphosate and conventional herbicides when used with glyphosatetolerant and non-tolerant crops. Environ Pollut 158:3172–3178
Masangkay RF, Paulitz TC, Hallett SG, Watson AK (2000) Solid substrate production of Alternaria alternata f. sp. sphenocleae conidia. Biocontrol Sci Techn 10:399–409
Masteling R, Lombard L, Boer WD, Raaijmakers JM, Dini-Andreote F (2019) Harnessing the microbiome to control plant parasitic weeds. Curr Opin Microbiol 49:23–33
Mitchell JK, Njalamimba-Bertsch M, Bradford NR, Birdsong JA (2003) Development of a submerged-liquid sporulation medium for the johnsongrass bioherbicide Gloecercospora sorghi. J Ind Microbiol Biot 30:599–605
Müller-Stöver D, Kohlschmid E, Sauerborn J (2009) A novel strain of Fusarium oxysporum from Germany and its potential for biocontrol of Orobanche ramose. Weed Res 49:175–182
Okunowo WO, Osuntoki AA, Adekunle AA, Gbenle GO (2013) Occurrence and effectiveness of an indigenous strain of Myrothecium roridum Tode: Fries as a bioherbicide for water hyacinth (Eichhornia crassipes) in Nigeria. Biocontrol Sci Techn 23:1387–1401
Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259
Phattanawasin P, Pojchanakom K, Sotanaphun U, Piyapolrungroj N, Zungsontiporn S (2007) Weed growth inhibitors from Aspergillus fischeri TISTR 3272. Nat Prod Res 21:1286–1291
Piyaboon O, Pawongrat R, Unartngam J, Chinawong S, Unartngam A (2016) Pathogenicity, host range and activities of a secondary metabolite and enzyme from Myrothecium roridum on water hyacinth from Thailand. Weed Biol Manag 16:132–144
Powles SB (2008) Evolved glyphosate-resistant weeds around the world: lessons to be learnt. Pest Manag Sci 64:360–365
Qiang S (2010) Current status and development strategy for weed science in China. Plant Prot 36:1–5
Qiang S, Wang L, Wei R, Zhou B, Chen SG, Zhu YZ, Dong YF, An CF (2010) Bioassay of the herbicidal activity of AAC-Toxin produced by Alternaria alternata isolated from Ageratina adenophora. Weed Technol 24:197–201
Rodriguez RJ, White-Jr JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Saikkonen K, Ruokolainen K, Huitu O, Gundel PE, Piltti T, Hamilton CE, Helander M (2013) Fungal endophytes help prevent weed invasions. Agric Ecosyst Environ 165:1–5
Shabana YM, Charudattan R, Tabl AHA, Morales-Payan JP, Rosskopf EN, Klassen W (2010) Production and application of the bioherbicide agent Dactylaria higginsii on organic solid substrates. Biol Control 54:159–165
Sica VP, Figueroa M, Raja HA, El-Elimat T, Darveaux BA, Pearce CJ, Oberlies NH (2016) Optimizing production and evaluating biosynthesis in situ of a herbicidal compound, mevalocidin, from Coniolariella sp. J Ind Microbiol Biotechnol 43:1149–1157
Silman RW, Nelsen TC (1993) Optimization of liquid culture medium for commercial production of Colletotrichum truncatum. FEMS Microbiol Lett 107:273–278
Silva NID, Brooks S, Lumyong S, Hyde KD (2018) Use of endophytes as biocontrol agents. Fungal Biol Rev 33:133–148
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis Version 6.0. Mol Biol Evol 30:2725–2729
Tang W, Zhu YZ, He HQ, Qiang S, Auld BA (2011) Field evaluation of Sclerotium rolfsii, a biological control agent for broadleaf weeds in dry, direct-seeded rice. Crop Prot 30:1315–1320
Teshler MP, Ash GJ, Zolotarov Y, Watson AK (2007) Increased shelf life of a bioherbicide through combining modified atmosphere packaging and low temperatures. Biocontrol Sci Techn 17:387–400
Tessmann DJ, Charudattan R, Preston JF (2008) Variability in aggressiveness, cultural characteristics, cercosporin production and fatty acid profile of Cercospora piaropi, a biocontrol agent of water hyacinth. Plant Pathol 57:957–966
Wang GP, Wang LW, Zhang YL, Wang JY, Xu XH, Zhang CL (2012a) Identification of an endophytic fungus of Ginkgo biloba TMSF169 and its antifungal metabolites. Chin J Biol Control 28:226–234
Wang J, Luo GJ, Meng YT, Liu L, Ye M, Fan LM, Zha YG (2013a) Isolation of endophytic bacteria from Eupatorium adenophorum and the herbicidal activity of their metabolites. Jiangsu Agric Sci 41:99–101
Wang J, Yi XH, Wei Y, Hao SH (2013b) Pesticide activity and molecular biology identification of 11 strains of endophytic fungi from Platycladus orientalis (L.) Franco. Chin Agric Sci Bull 15:183–187
Wang LW, Xu BG, Wang JY, Su ZZ, Lin FC, Zhang CL, Kubicek CP (2012b) Bioactive metabolites from Phoma species, an endophytic fungus from the Chinese medicinal plant Arisaema erubescens. Appl Microbiol Biotechnol 93:1231–1239
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications, vol 18. Academic Press Inc., San Diego, CA, USA, pp 315–322
Woudenberg JHC, Seidl MF, Groenewald JZ, de Vries M, Stielow JB, Thomma BPHJ, Crous PW (2015) Alternaria section Alternaria: Species, formae speciales or pathotypes? Stud Mycol 82:1–21
Xu CP, Kim SW, Hwang HJ, Choi JW, Yun JW (2003) Optimization of submerged culture conditions for mycelial growth and exo-biopolymer production by Paecilomyces tenuipes C240. Process Biochem 38:1025–1030
Yirefu F, Struik PC, Lantinga EA, Tessema T (2017) Occurrence and diversity of fungal pathogens associated with water hyacinth and their potential as biocontrol agents in the Rift Valley of Ethiopia. Int J Pest Manage 63:1–9
Zhu YZ, Qiang S (2004) Isolation, pathogenicity and safety of Curvularia eragrostidis isolate QZ-2000 as a bioherbicide agent for large crabgrass (Digitaria sanguinalis). Biocontrol Sci Techn 14:769–782
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant No.31760539; 31160371; 30860165; 31560518), the Project of Science and Technology Department of Qinghai Province, China (Grant No. 2018-ZJ-917), Key Laboratory Project on Agricultural Integrated Pest Management of Qinghai Province(Grant No.2020-ZJ-Y11), and The second Tibetan Plateau Scientific Expedition and Research Program (Grant No.2019QZKK0303).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cheng, L., Zhu, H.X., Wei, Y.H. et al. Biological control of Qinghai plateau terrestrial weeds with the A. alternata HL-1. J Plant Dis Prot 128, 1691–1704 (2021). https://doi.org/10.1007/s41348-021-00514-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41348-021-00514-2