The origin of the agriculture was one of the turning points in human history, and a central part of this was the evolution of new plant forms, domesticated crops. Seed dispersal and germination are two key traits which have been selected to facilitate cultivation and harvesting of crops. The objective of this study was to analyze anatomical structure of seed coat and pod, identify metabolic compounds associated with water-impermeable seed coat and differentially expressed genes involved in pea seed dormancy and pod dehiscence. Comparative anatomical, metabolomics, and transcriptomic analyses were carried out on wild dormant, dehiscent Pisum elatius (JI64, VIR320) and cultivated, indehiscent Pisum sativum non-dormant (JI92, Cameor) and recombinant inbred lines (RILs). Considerable differences were found in texture of testa surface, length of macrosclereids, and seed coat thickness. Histochemical and biochemical analyses indicated genotype related variation in composition and heterogeneity of seed coat cell walls within macrosclereids. Liquid chromatography–electrospray ionization/mass spectrometry and Laser desorption/ionization–mass spectrometry of separated seed coats revealed significantly higher contents of proanthocyanidins (dimer and trimer of gallocatechin), quercetin, and myricetin rhamnosides and hydroxylated fatty acids in dormant compared to non-dormant genotypes. Bulk Segregant Analysis coupled to high throughput RNA sequencing resulted in identification of 770 and 148 differentially expressed genes between dormant and non-dormant seeds or dehiscent and indehiscent pods, respectively. The expression of 14 selected dormancy-related genes was studied by qRT-PCR. Of these, expression pattern of four genes: porin (MACE-S082), peroxisomal membrane PEX14-like protein (MACE-S108), 4-coumarate CoA ligase (MACE-S131), and UDP-glucosyl transferase (MACE-S139) was in agreement in all four genotypes with Massive analysis of cDNA Ends (MACE) data. In case of pod dehiscence, the analysis of two candidate genes (SHATTERING and SHATTERPROOF) and three out of 20 MACE identified genes (MACE-P004, MACE-P013, MACE-P015) showed down-expression in dorsal and ventral pod suture of indehiscent genotypes. Moreover, MACE-P015, the homolog of peptidoglycan-binding domain or proline-rich extensin-like protein mapped correctly to predicted Dpo1 locus on PsLGIII. This integrated analysis of the seed coat in wild and cultivated pea provides new insight as well as raises new questions associated with domestication and seed dormancy and pod dehiscence.
There is growing interest in the conservation and utilization of crop wild relatives (CWR) in international food security policy and research. Legumes play an important role in human health, sustainable food production, global food security, and the resilience of current agricultural systems. Pea belongs to the ancient set of cultivated plants of the Near East domestication center and remains an important crop today. Based on genome-wide analysis, P. fulvum was identified as a well-supported species, while the diversity of wild P. sativum subsp. elatius was structured into 5 partly geographically positioned clusters. We explored the spatial and environmental patterns of two progenitor species of domesticated pea in the Mediterranean Basin and in the Fertile Crescent in relation to the past and current climate. This study revealed that isolation by distance does not explain the genetic structure of P. sativum subsp. elatius in its westward expansion from its center of origin. The genetic diversity of wild pea may be driven by Miocene-Pliocene events, while the phylogenetic diversity centers may reflect Pleisto-Holocene climatic changes. These findings help set research and discussion priorities and provide geographical and ecological information for germplasm-collecting missions, as well as for the preservation of extant diversity in ex-situ collections.
Pea, one of the founder crops from the Near East, has two wild species: Pisum sativum subsp. elatius, with a wide distribution centered in the Mediterranean, and P. fulvum, which is restricted to Syria, Lebanon, Israel, Palestine and Jordan. Using genome wide analysis of 11,343 polymorphic single nucleotide polymorphisms (SNPs) on a set of wild P. elatius (134) and P. fulvum (20) and 74 domesticated accessions (64 P. sativum landraces and 10 P. abyssinicum), we demonstrated that domesticated P. sativum and the Ethiopian pea (P. abyssinicum) were derived from different P. elatius genepools. Therefore, pea has at least two domestication events. The analysis does not support a hybrid origin of P. abyssinicum, which was likely introduced into Ethiopia and Yemen followed by eco-geographic adaptation. Both P. sativum and P. abyssinicum share traits that are typical of domestication, such as non-dormant seeds. Non-dormant seeds were also found in several wild P. elatius accessions which could be the result of crop to wild introgression or natural variation that may have been present during pea domestication. A sub-group of P. elatius overlaps with P. sativum landraces. This may be a consequence of bidirectional gene-flow or may suggest that this group of P. elatius is the closest extant wild relative of P. sativum.
Knowledge of current genetic diversity and mating systems of crop wild relatives (CWR) in the Fertile Crescent is important in crop genetic improvement, because western agriculture began in the area after the cold-dry period known as Younger Dryas about 12,000 years ago and these species are also wild genepools of the world’s most important food crops. Wild pea (Pisum sativum subsp. elatius) is an important source of genetic diversity for further pea crop improvement harbouring traits useful in climate change context. The genetic structure was assessed on 187 individuals of Pisum sativum subsp. elatius from fourteen populations collected in the northern part of the Fertile Crescent using 18,397 genome wide single nucleotide polymorphism DARTseq markers. AMOVA showed that 63% of the allelic variation was distributed between populations and 19% between individuals within populations. Four populations were found to contain admixed individuals. The observed heterozygosity ranged between 0.99 to 6.26% with estimated self-pollination rate between 47 to 90%. Genetic distances of wild pea populations were correlated with geographic but not environmental (climatic) distances and support a mixed mating system with predominant self-pollination. Niche modelling with future climatic projections showed a local decline in habitats suitable for wild pea, making a strong case for further collection and ex situ conservation.
Seed coats serve as protective tissue to the enclosed embryo. As well as mechanical there are also chemical defence functions. During domestication, the property of the seed coat was altered including the removal of the seed dormancy.We used a range of genetic, transcriptomic, proteomic and metabolomic approaches to determine the function of the pea seed polyphenol oxidase (PPO) gene. Sequencing analysis revealed one nucleotide insertion or deletion in the PPO gene, with the functional PPO allele found in all wild pea samples, while most cultivated peas have one of the three nonfunctional ppo alleles. PPO functionality cosegregates with hilum pigmentation. PPO gene and protein expression, as well as enzymatic activity, was downregulated in the seed coats of cultivated peas.The functionality of the PPO gene relates to the oxidation and polymerisation of gallocatechin in the seed coat. Additionally, imaging mass spectrometry supports the hypothesis that hilum pigmentation is conditioned by the presence of both phenolic precursors and sufficient PPO activity.Taken together these results indicate that the nonfunctional polyphenol oxidase gene has been selected during pea domestication, possibly due to better seed palatability or seed coat visual appearance.
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