Genus-wide screening of Vigna reveals an evolutionary pattern of high biotic vs. low abiotic stress resilience
Our findings show that sources of pest and disease resistance occur in at least 75 percent of the taxa, which were part of screening assessments. In contrast, sources of abiotic stress resilience occur in less than 30 percent of the taxa, which were part of screening assessments. We therefore hypothesize that during evolution, Vigna taxa have been conservative in acquiring traits related to abiotic stress resilience compared with pest and diseases resistance. To verify the pattern of high biotic vs. low abiotic stress resilience for the whole Vigna it is necessary to screen more Vigna taxa from gene pools C and D, which belong both to Vigna subgenus Vigna because these are under-represented in the screening studies, which were reported in this study.
Fifteen percent of the taxa screened in the ecogeographic analysis occur in seasonally hot or seasonally dry climate conditions, where it is possible to escape heat and drought stress through rapid flowering and maturation rather than to tolerate heat and drought stress. In contrast, five percent of the taxa occurs in permanently hot or permanently dry climate conditions, and requires traits to tolerate continuous heat or drought stress. This finding suggests that during evolution Vigna taxa more easily acquire phenological traits for short life cycles to escape drought and heat stresses compared with acquiring physiological traits to tolerate these stresses continuously.
Co-evolution can explain the high percentage of taxa, which possesses biotic stress resistance compared with heat and drought stress resilience. Resistance against pest and diseases has often been a result from continuous and recent co-evolution in the geographic areas of occurrence and pressure of pest and diseases43. Pest pressure can change genotype frequencies in a plant population within just a few generations44,45. For example for wild tomato relatives, the density of trichomes and levels of acylsugar concentrations, related to direct pest defence, correspond with pest pressure and the geographic distribution of these pests46,47.
The presence of salinity tolerance in 27 percent of taxa compared with eight percent drought-tolerant taxa in the pot experiments, suggest that Vigna taxa are good at developing salt-tolerant traits compared with drought-tolerant traits16. Several wild Vigna taxa occur naturally in coastal areas and are adapted to a saline environment41. These Vigna genetic resources are of high value for legume production in geographic areas, which suffer from salinization.
Our findings suggest that the section Aconitifolia contains high levels of heat and drought stress resilience. This section includes V. aconitifolia (moth bean), which occurs in permanently dry and seasonally hot climate conditions. This finding contrasts with the low dehydration tolerance of V. aconitifolia, which was reported in the pot experiments11. Two possible reasons can explain this discrepancy. First, the pot experiment measured dehydration tolerance at an early growth stage while plants can have traits to tolerate or escape drought stress during all growth stages. The ecogeographic analysis captures this broad range of traits with presence records of populations of V. aconitifolia in harsh environments. Second, the limited number of accessions of V. aconitifolia in the pot experiments may not reflect the full intra-specific genetic variation of this species.
Vice versa, V. aridicola from section Aconitifoliae tolerated dehydration while the ecogeographic analysis indicated that this species occurs in humid regions. It could be that our analysis does not reflect the complete climatic ranges because we only were able to collect 14 presence records of this species.
Numerous Vigna taxa from all four gene pools occur in marginal conditions, on poor sandy soils, or geographic areas that are regularly inundated41, 42. We therefore anticipate that many Vigna taxa, which have not been phenotyped for abiotic stress resilience yet, have traits related to abiotic stress resilience. The biggest phenotyping gap is in the Vigna taxa of gene pools C and D, which belong both to Vigna subgenus Vigna.
To test if the pattern of high biotic vs. low abiotic stress resilience is common in gene pools of other legume crops, more screening studies are required that simultaneously assess abiotic or biotic stress resilience. We only found one study, which simultaneously screened legume wild relatives for abiotic stress and biotic stress resilience48. This study with eight chickpea wild relatives (Cicer spp.) focuses on cold stress rather than heat stress in combination with biotic stress resistance. Nevertheless, the study’s results are in line with our findings of high biotic vs. low abiotic stress resilience because the researchers identified four or more Cicer taxa resisting bruchids and other pests and diseases compared with only two wild Cicer taxa tolerating cold stress.
Identification of multifunctional traits
Because of the high frequency of taxa with traits related to biotic stress resilience, we expect that taxa with traits related to abiotic stress resilience have also a high chance to include traits related to biotic stress resilience. Our analysis suggests that many taxa from the section Aconitifoliae show high levels of abiotic stress resilience, but only a limited number of accessions from this section were screened for resistance against pests and diseases. These and other Vigna taxa with high levels of abiotic stress resilience would require further evaluation under different abiotic and biotic stress combinations.
To date, screening and understanding of the ability of Vigna taxa to adapt against combined biotic and abiotic stresses is largely unknown. Taxa, which are adapted to hot, drought, or extreme-rainfall conditions could have stacked different traits over time to cope with both abiotic and biotic stresses. In addition, multifunctional traits, such as high levels of antioxidant capacity, could help these taxa to tolerate abiotic and biotic stresses at the same time49. In fact, exaptation, which is the evolutionary process of changes in trait functions50, predicts that a trait, which initially responded to a single stress, is likely to generate several functions over evolutionary time to eventually respond to multiple stresses.
We propose trichomes as a promising multifunctional trait in Vigna taxa for further screening because trichomes help plants to cope with both abiotic and biotic stresses51. High density of trichomes on the pods of V. radiata and the V. unguiculata complex complicates the mobility of the adult of bruchids and pod borers over the pods and decrease pest infestations18,52. Numerous studies show that glandular trichomes in tomato wild relatives produce secondary metabolites including acylsugars, methylketones, and sesquiterpenes, which intoxicate, repel, or trap pests19,53. At the same time, trichomes may increase abiotic stress tolerance by reducing leaf radiation absorbance and facilitate condensation of air moisture onto the plant surface, among other functions54. Further research will reveal the relationships between trichomes types and densities, trichrome evolution, and abiotic and biotic stress resilience in Vigna taxa.
Cross-compatibility between Vigna taxa is poorly understood
For many Vigna taxa, genetic relationships and crossing compatibility are still poorly understood. This is especially true for the pantropical Vigna section of subgenus Vigna, which includes taxa from Africa, the Americas, and the Pacific. Domestication and origin of Vigna taxa is largely unknown. For example, where did the Vigna genus originate and how did the genus spread across Africa, Asia, the Americas, and the Pacific?
Only few studies reported on biotic stress resilience of wild relatives of V. unguiculata (cowpea) compared with wild relatives of V. radiata (mung bean). It could be that cowpea breeders do not yet need to use wild relatives of the V. unguiculata complex for biotic stress resilience because the many botanical varieties in the primary gene pool of the V. unguiculata complex provide sufficient variation for finding traits. Another possibility could be that V. unguiculata is difficult to cross with close relatives compared with V. radiata and its close relatives, which requires further crossing studies.
Quarter of Vigna taxa requires urgent conservation actions
Twenty-six percent of the 88 Vigna taxa, which were considered in this study, requires urgent germplasm collecting efforts because they are not- or under-represented in genebanks. Two Asian Vigna taxa and four African Vigna taxa require urgent efforts of germplasm collecting because no genebank had reported the maintenance of these taxa. Nine other Asian Vigna taxa and seven other African Vigna taxa also require urgent efforts of germplasm collecting because genebanks reported less than 10 accessions of these taxa. Targeted Asian and Pacific countries for germplasm collecting efforts include India, Thailand, Myanmar, Sri Lanka, Australia, and Taiwan. In Africa, our sampled and modelled richness analyses indicate Burundi, Benin, DRC Congo, and Madagascar as priority countries for Vigna germplasm collecting efforts..
Vigna taxa with high levels of heat and drought stress tolerance are rare. We therefore propose to use the presence of these type of traits as a criterion to prioritize taxa for conservation. The section Aconitifoliae requires urgent conservation efforts when considering this criterion in combination with poor genebank coverage. Five out of the seven Aconitifoliae taxa are poorly conserved ex situ with 10 or fewer reported accessions in genebanks while this section includes several traits related to abiotic stress tolerance. Taxa from this section mainly occur in India and Sri Lanka, which are priority countries for germplasm collecting. In addition to the taxa in this section, Vigna exilis, which occurs in permanently hot climate conditions and V. monantha, which occurs in permanently dry conditions, also require urgent conservation because these taxa were not reported in genebanks, except for one accession of V. exilis.
The pacific V. o-wahuensis, endemic to Hawaii, is critically endangered according to the U.S. Endangered Species Act56. Fortunately, 27 accessions have been safeguarded in the Lyon Arboretum, Hawaiian Rare Plant Program (pers. comm. Marian Chau, Lyon Arboretum). Strengthening collaboration between genebanks and botanical gardens such as the Lyon Arboretum and the National Botanic Garden of Belgium in Meise, would further enhance ex situ conservation and germplasm availability of Vigna.
Vigna monantha and another African Vigna, V. keraudrenii require urgent in situ and ex situ conservation efforts because these taxa are endangered according to the IUCN Red List55. Until now, the IUCN has evaluated only six Vigna taxa as part of the Red List. The inclusion of more Vigna taxa on the IUCN Red List will help to understand their in situ conservation status better.
Source: Ecology - nature.com
