Multiple post-domestication origins of kabuli chickpea through allelic variation in a diversification-associated transcription factor

Authors: PENMETSA, R - University Of California; CARRASQUILLA-GARCIA, N - University Of California; BERGMANN, E - University Of California; VANCE, L - University Of California; CASTRO, B - University Of California; KASSA, M - University Of California; SARMA, B - University Of California; DATTA, S - University Of California; FARMER, A - National Center For Genome Resources; BAEK, J - University Of California; Coyne, Clarice - Clare; VARSHNEY, R - International Crops Research Institute For Semi-Arid Tropics (ICRISAT) - India; VON WETTBERG, E J - Florida International University; COOK, D - University Of California

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/24/2016
Publication Date: 5/19/2016
Citation: Penmetsa, R.V., Carrasquilla-Garcia, N., Bergmann, E.M., Vance, L., Castro, B., Kassa, M.T., Sarma, B.K., Datta, S., Farmer, A.D., Baek, J.M., Coyne, C.J., Varshney, R.K., Von Wettberg, E.B., Cook, D.R. 2016. Multiple post-domestication origins of kabuli chickpea through allelic variation in a diversification-associated transcription factor. New Phytologist. 211:1440-1451.

Interpretive Summary: Domestication is the adaptation through human selection of wild species for use in human-shaped environments. Novel genetic variants, detrimental in nature but superior in agricultural settings are typically the genetic basis of domesticated forms. Chickpea is among the founder crops domesticated in the Fertile Crescent at the advent of agriculture. One of two major forms of chickpea, the ‘kabuli’ type, has light-colored flowers and seed coats, properties selected by humans and not known to exist in the wild progenitors. We determined that a bHLH transcription factor, orthologous to Mendel’s A gene of garden pea, conditions this light-colored trait in chickpea. Its functional loss underlies multiple origins of kabuli chickpea, subsequent to primary domestication.

Technical Abstract: Chickpea (Cicer arietieum) is a widely cultivated food legume and one of the Neolitic founder crops domesticated in the Fertile Crescent. Cultivated chickpea is classified into two types, a ‘desi’ type with smaller and darker seed coats, and a light-colored large-seeded ‘kabuli’ type, with the two types commonly viewed as genetically distinct. Analyses of multi-locus bi-allelic nucleotide polymorphisms in 538 genes across chickpea germplasm substantiate a reduction in genetic diversity in cultivated chickpea, implicate extensive genetic admixture within cultivated chickpea and its wild progenitor, and indicate multiple origins of the kabuli type. We identified a basic helix-loop-helix (bHLH) transcription factor at the genetically defined B locus, variation in which co-segregates in a recombinant inbred population invariantly with the white flower and light seed coat color phenotypes of kabuli chickpea. Among 178 diverse domesticated accessions, kabuli but not desi chickpea are associated with coding region variation in this transcription factor, an ortholog of the Mendel's A gene of garden pea (Pisum sativum). Four loss-of-function and a fifth reduced-function variant of the bHLH transcription factor occur exclusively in kabuli chickpea, being accompanied by attenuated expression of leucoanthocyanidin dioxygenase and anthocyanidin reductase in petal and seed coat tissues. The concordance between the polyphyletic distribution of the kabuli form in germplasm, and the absence of nested allelic variation at the bHLH gene, strongly suggest that the kabuli type arose multiple times during the phase of phenotypic diversification after initial domestication of cultivated chickpea from the wild annual relative Cicer reticulatum.