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Koce, J.D.; Kocjan, D. Genome Size and Life Forms of Araceae. Encyclopedia. Available online: https://encyclopedia.pub/entry/19067 (accessed on 02 May 2024).
Koce JD, Kocjan D. Genome Size and Life Forms of Araceae. Encyclopedia. Available at: https://encyclopedia.pub/entry/19067. Accessed May 02, 2024.
Koce, Jasna Dolenc, Domen Kocjan. "Genome Size and Life Forms of Araceae" Encyclopedia, https://encyclopedia.pub/entry/19067 (accessed May 02, 2024).
Koce, J.D., & Kocjan, D. (2022, February 01). Genome Size and Life Forms of Araceae. In Encyclopedia. https://encyclopedia.pub/entry/19067
Koce, Jasna Dolenc and Domen Kocjan. "Genome Size and Life Forms of Araceae." Encyclopedia. Web. 01 February, 2022.
Genome Size and Life Forms of Araceae
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This entry is adapted from the peer-reviewed paper 10.3390/plants11030334

The genome size of an organism is an important trait that has predictive values applicable to various scientific fields, including ecology. The main source of plant C-values is the Plant DNA C-values database of the Royal Botanic Gardens Kew, which currently contains 12,273 estimates. However, it covers less than 3% of known angiosperm species and has gaps in the life form and geographic distribution of plants. New C-values for the aroid family (Araceae), collected in the Piedras Blancas National Park area in southern Costa Rica, including terrestrial, epiphytic and aquatic life forms are combined with C-value entries in the RBGK database for Araceae. The analysis reveals a wider range of C-values for terrestrial aroids, consistent with other terrestrial plants, a trend toward slightly lower C-values for epiphytic forms, which is more consistent for obligate epiphytes, and comparatively low C-values for aquatic aroids.

aquatic plant aroid epiphyte nuclear DNA amount terrestrial plant

1. Introduction

Genome size is a term widely used in the scientific literature, but it is used with different meanings depending on the author [1]. Authors use it here as a term that expresses the amount of DNA in the nucleus of a cell. The nuclear DNA amount is usually expressed as what is called the C-value, where “C” stands for “constant” [2]. The 1C-value refers to the size of the haploid genome, regardless of chromosome numbers and degree of polyploidy. Such a genome is found in an unduplicated nucleus of a haploid gamete. The 2C-value refers to the nuclear DNA amount in a duplicated nucleus of a gamete and an unduplicated nucleus of a diploid somatic cell. The 4C-value refers to the amount of nuclear DNA in a duplicated diploid nucleus before mitosis or meiosis. C-values higher than 4C are results of endopolyploidy [3], with the highest known multiplication being 24,576 C, as measured in the endosperm of the aroid Arum maculatum [4].
The C-value varies greatly among species. There is no correlation between the complexity of an organism and its genome size. This was known as the “C-value paradox” before the discovery of noncoding DNA [5][6]. Although knowledge of the importance of genome size has improved in recent decades, the source of the extensive variation in nuclear genome size among eukaryotic species and the functional significance of the genome size remain largely unsolved. This puzzle is known as the “C-value enigma”, as described by Gregory [7].
Currently, there are three main hypotheses that attempt to explain the importance of genome size variations in organisms. The first hypothesis is that the variation is a random effect of mutations that duplicate and accumulate so-called nonessential or “selfish” DNA [8]. Species with larger genomes are thought to be those that better tolerate the accumulation of “selfish” DNA. Therefore, genome size, and the resulting larger cell size, are not of biological importance [6]. The second hypothesis is the so-called nucleotype hypothesis. The term nucleotype was formed as a counterpart to genotype. It is designed to describe the influence of the nucleus on the phenotype, which is based on the size and structure of the DNA, independent of the genes encoded in the DNA [9]. According to this hypothesis, genome size has an active biological role in an organism, and its life cycle is particularly correlated with genome size. The final hypothesis, called the nucleoskeletal hypothesis, states that cell size has an active biological role while genome size is a passive consequence of cell growth. A larger amount of DNA would primarily have the role of a nucleoskeleton to help to maintain an optimized ratio between the nucleus and cytoplasm, thereby optimizing cell processes [10][11].
Genome size is useful in a variety of disciplines, from molecular biology, taxonomy, evolutionary biology, phylogeny and ecology, to conservation [12]. More than 20 years ago, it was proposed that the nuclear DNA amount in vascular plants can be used to predict vegetation responses to landscape and climate change by linking genome size variations to ecological patterns and processes [13]. To test predictions of vegetation responses to climate and land use at different geographic scales, a need for appropriate data collection was also identified at that time. Based on the idea of improving the accessibility of plant genome sizes by making them available for reference purposes in the form of published reference lists and/or on the Internet in a database of plant DNA C-values, an open-access database that is maintained by the Royal Botanic Gardens Kew, UK (RBGK) [14], was released in 2001.
The RBGK database currently contains 12,273 C-value estimates from different plant groups [14] and are expressed as the number of base pairs (bp) or as the mass of DNA in picograms (1 pg = 10−12 g) where one picogram is approximately 109 base pairs [15]. In angiosperms, the C-values range from 1C = 0.06 pg to 1C = 150 pg. However, current C-value estimates represent only 2.9% of the C-values of the 369,434 known angiosperm species [16]. In addition to taxonomic inadequacies, this knowledge of genome size includes geographic inadequacies. In 2011, Bennett and Leitch [17] showed that 58.2% of all genome data were reported by European researchers, with only 4.5% from Central and South America. There is also insufficient data for certain life forms, such as epiphytes.
Aroids (Araceae) are the third largest family of monocots, which comprise ca. 140 genera [18] with around 4000 species described [19]. These are spread all over the globe (Figure 1), but over 90% of species are found in the tropics [20]. The most diverse regions are Central and South America, Southeast Asia, the Malay Archipelago and continental tropical Africa. Most species are found in the tropics of Central and South America. Many species are endemic, while some are widespread [21]. Members of the aroid family are found in a variety of different habitats, from tropical dry to pluvial rainforest, through tropical swamps and cloud forests, to subarctic marshes and montane plains [22].
Figure 1. The global distribution of Araceae. Values in black indicate the percentage of aroid species on each continent, with distribution data taken from Plants of the World Online [18]. Values in red indicate the percentage of known aroid C-values for each continent, with data from the RBGK database [14].
Most aroids are terrestrial. Many are geophytes with spreading rhizomes [21][22] or climbers that require external support [23]. However, both geophytes and climbers require a root connection to the soil.
A common life form of aroids is epiphytes. These plants grow on a host plant and do not require ground contact to survive. Epiphytes obtain all of their required nutrients and water from precipitation and leaf litter. The so-called litter-basket epiphytes can collect water and leaf litter due to their shape and leaf arrangement [21]. Among the aroids, there are obligate epiphytes (e.g., Anthurium obtusum), which are exclusively epiphytic, and facultative epiphytes (e.g., Philodendron auriculatum), which can also grow on the ground [24]. The facultative epiphytes thrive in habitats such as cloud forests, where living conditions on the ground and on host plants are similar. Hemiepiphytic aroids (e.g., Anthurium gymnopus) germinate as epiphytes, then sprout feeder roots that reach the ground [21][25]. Some studies have also recognized secondary hemiepiphytes, although more recent studies [23][24] recommend the term nomadic vines or nomadic climbers (a term that is further used in this entry). These germinate as terrestrial plants, then begin climbing on a host plant and eventually lose contact with the soil as their initial roots die (e.g., Monstera adansonii). The plant only remains connected to the soil through its adventitious roots [23][24][26].
Depending on how much they depend on constant contact with water, various life forms of aroids can be considered aquatic. They can be floating aquatic plants (e.g., Lemna minor) or submerged aquatic plants (e.g., Cryptocoryne crispatula). These grow in water bodies and can be free-floating or rooted in the substrate, whereas rheophytes (e.g., Anthurium amnicola) grow on rocks in waterways, and helophytes (e.g., Orontium aquaticum) are wetland plants that grow in waterlogged soil [21]. This becomes more complicated when it is considered that epiphytic plants can also grow on rocks rather than host plants. These are epilithic, but this form is optional in virtually all juvenile epiphytes. Rheophytes can also be considered epilithic, although they are also aquatic [22].
Of the approximately 4000 known aroid species [19], C-values are known for less than 4% of them, and most of them are already included in the RBGK C-value database [14]. While the number of C-value estimates in the RBGK C-value database (Figure 1) covers most aroids in Africa, Asia and Australia, it is overestimated in Europe and North America, likely due to repeated measurements of the C-value in the same plant. In comparison, the number of C-value entries in the database is 10 times lower (i.e., 35%) for Central and South America than would be expected given the number of aroids in the area.
To fill an important part of the identified life-form-specific and geographic gaps in the C-value database for aroids, terrestrial and various epiphytic forms of aroids originating from the area of Piedras Blancas National Park in southern Costa Rica [27] were analyzed together with the existing data in the C-value database to reveal a possible relationship between the C-value and a specific life form of the aroids.

2. C-Value Estimates

Forty-one new C-values from six aroid life forms (Figure 2) were estimated with DNA image cytometry (Table 1). These include 26 epiphytic aroid forms, which represent almost 60% of all of the data on epiphytic aroids previously included in the RBGK C-value database [14]. New C-value estimates include those of five genera measured for the first time (Adelonema, Aglaonema, Dracontium, Rhodospatha, Stenospermation), as well as data from wild forms of the genus Spathiphyllum, for which C-values were previously measured only for their horticultural cultivars [28][29]. Authors also measured C-values already recorded in the database [14] for obligatory epiphytes Anthurium clavigerum and A. obtusum, a facultative epiphyte A. hoffmanii, three terrestrial species Alocasia longiloba, Anthurium ochranthum and Xanthosoma sagittifolium, a nomadic vine Syngonium podophyllum, and an aquatic species Pistia stratiotes.
Figure 2. Life forms of the Araceae collected in the Piedras Blancas National Park area: (A) Aquatic plant (Pistia stratiotes); (B) Nomadic vine (Philodendron pterotum); (C) Obligatory epiphyte (Anthurium ravenii); (D) Facultative epiphyte (Anthurium hoffmanii); (E) Terrestrial plant (Adelonema erythropus).
Table 1. Details of the aroids collected in the Piedras Blancas National Park area, with information on their life form and genome size measurements (mean 2C-value ± standard error).
Genus Species Life Form 2C ± SE [pg DNA]
Adelonema A. erythropus Terrestrial 3.50 ± 0.12
A. wendlandii Terrestrial 3.51 ± 0.08
Aglaonema A.cf. marantifolium Terrestrial 62.48 ± 2.70
Alocasia A. longiloba Terrestrial 27.50 ± 0.70
A. clypeolata Terrestrial 11.02 ± 0.30
Anthurium A. brownii Obligatory epiphyte 8.45 ± 0.10
A. clavigerum Obligatory epiphyte 13.23 ± 0.15
A. hacumense Obligatory epiphyte 8.09 ± 0.20
A. hoffmanii Facultative epiphyte 7.83 ± 0.20
A. obtusum Obligatory epiphyte 5.54 ± 0.10
A. ochranthum Terrestrial 12.48 ± 0.30
A. cf. ravenii Obligatory epiphyte 8.63 ± 0.20
Dieffenbachia D. concinna Terrestrial 33.13 ± 0.30
Dracontium D. pittieri Terrestrial 10.17 ± 0.10
Monstera M. adansonii Nomadic vine 10.54 ± 0.46
M. gambensis Nomadic vine 9.21 ± 0.20
M. pinnatipartita Nomadic vine 12.04 ± 0.30
Philodendron P. auriculatum Facultative epiphyte 3.23 ± 0.10
P. fragrantissimum Nomadic vine 4.86 ± 0.10
P. grandipes Terrestrial 4.30 ± 0.10
P. mexicanum Nomadic vine 3.65 ± 0.20
P. microstictum Nomadic vine 3.56 ± 0.00
P. opacum Nomadic vine 3.07 ± 0.10
P. platypetiolatum Nomadic vine 3.55 ± 0.10
P. popenoei Terrestrial 2.90 ± 0.00
P. pterotum Nomadic vine 5.12 ± 0.10
P. sagittifolium Nomadic vine 3.60 ± 0.00
P. rhodoaxis Nomadic vine 2.54 ± 0.10
P. sp. Facultative epiphyte 3.28 ± 0.10
P. tripartitum Nomadic vine 3.78 ± 0.10
Pistia P. stratiotes Aquatic 0.83 ± 0.00
Rhodospatha R. osaensis Nomadic vine 3.09 ± 0.27
R. cf. osaensis Nomadic vine 2.54 ± 0.00
Spathiphyllum S. cf.leave Terrestrial 22.12 ± 0.30
S. silvicola Terrestrial 18.29 ± 0.50
S. wendlandii Terrestrial 20.07 ± 0.40
Stenospermation S. angustifolium Obligatory epiphyte 7.49 ± 0.20
S. cf. maranthifolium Obligatory epiphyte 7.24 ± 0.20
Syngonium S. hastiferum Nomadic vine 7.16 ± 0.20
S. podophyllum Nomadic vine 5.48 ± 0.10
Xanthosoma X. sagittifolium Terrestrial 4.81 ± 0.10

3. Aroid C-Values Related to Plant Life Forms

The new data were combined with the C-values from the RBGK database and the study of Zhao et al. [30]. Analysis of the C-values showed a moderately wide range of 2C-values among the aroids, which averaged out as 2.95 pg DNA for the aquatic aroids, and 15.26 pg DNA for the terrestrial aroids, with a trend toward an interestingly different distribution of 2C-values among the different aroid life forms (Figure 3).
Figure 3. The distribution of the 2C-values for each aroid life form. Each violin ranges from the minimum to the maximum value, and its shape represents the frequency distribution of the data. The lines mark the median values calculated for the number of measured samples (N).
Bennett [31] has shown that perennial herbs have a wide range of C-values, which is also mirrored for the terrestrial aroids in the present study. Their mean value is greater than 76% of all of the C-values analyzed (Figure 3). However, two species (Aglaonema cf. marantifolium, Zamioculcas zamiifolia) had significantly higher C-values than other terrestrials (Table 1, [29]).
Plants of different epiphytic types had similar 2C-values (Table 1, Figure 3). There was only one outlier among facultative epiphytes, namely Anthurium grande, and Scindapsus pictus in the nomadic vine group [32]. Obligatory epiphytes showed a more uniform distribution of 2C-values, with no major outliers. Whether this uniformity of C-values in epiphytic aroids is of any biological significance is not clear at present.
The aquatic forms had the smallest C-values among the aroids, and their C-values represented a small range at the lower end of the scale (Table 1, Figure 3). The genus Wolffia had the highest C-values among the aquatic aroids [33]. The C-values of species in the rooted genus Cryptocoryne were only slightly lower [29]. Two sizable outliers were detected, namely Anthurium amnicola and Anthurium antioquiense. Despite their rheophytic lifestyle in nature, they are also cultivated as terrestrial ornamentals, and their C-values were within the range of the large diversity of life forms within the entire genus Anthurium. Another outlier among the aquatic aroids was Orontium aquaticum [14] with high C-value which might be related to its distinct morphological and phylogenetic lineage. The low C-values of aquatic aroids might be related to the prevalence of rapid vegetative reproduction [34][35], which can promote opportunistic growth during episodes of suitable growing conditions [13].

References

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