Ancient relaxation of an obligate short-day requirement in common bean through loss of CONSTANS-like gene function

Ana M González,Jacqueline K Vander Schoor,Chao Fang,Fanjiang Kong,Jing Wu,James L Weller,Marta Santalla

doi:10.1016/j.cub.2021.01.075

Abstract

Common bean (Phaseolus vulgaris L.) is a major global food staple and source of dietary protein that was domesticated independently in Mexico and Andean South America. Its subsequent development as a crop of importance worldwide has been enabled by genetic relaxation of the strict short-day requirement typical of wild forms, but the genetic basis for this change is not well understood. Recently, a loss of photoperiod sensitivity was shown to result from mutations in the phytochrome photoreceptor gene Ppd/PHYA3 that arose independently within the two major domesticated lineages. Here, we define a second major photoperiod sensitivity locus, at which recessive alleles associate with deleterious mutations affecting the CONSTANS-like gene COL2. A wider survey of sequence variation in over 800 diverse lines, including wild, landrace, and domesticated accessions, show that distinct col2 haplotypes are associated with early flowering in Andean and Mesoamerican germplasm. The relative frequencies and distributions of COL2 and PHYA3 haplotypes imply that photoperiod adaptation developed in two phases within each gene pool: an initial reduction in sensitivity through impairment of COL2 function and subsequent complete loss through PHYA3. Gene expression analyses indicate that COL2 functions downstream of PHYA3 to repress expression of FT genes and may function in parallel with PvE1, the bean ortholog of a key legume-specific flowering repressor. Collectively, these results define the molecular basis for a key phenological adaptation, reveal a striking convergence in the naturally replicated evolution of this major crop, and further emphasize the wider evolutionary lability of CONSTANS effects on flowering time control.

Highlights

Common bean (Phaseolus vulgaris L.) has major significance as a staple food crop and source of dietary protein in many cultures around the world.[1]
Early photoperiod-insensitive flowering has arisen separately in Mesoamerican and Andean gene pools through distinct loss-of-function mutations in the phytochrome A gene Ppd.[14]. We show this was likely preceded by a partial loss of sensitivity conferred by mutations in the CONSTANS-like gene COL2 that are specific to each germplasm group
A major locus on chromosome 4 contributes to photoperiod sensitivity in common bean We previously identified the molecular basis for the photoperiod sensitivity locus Ppd in a study of F2 progeny from a cross between the Andean domesticated cultivar Midas and the Mesoamerican wild line G12873 (MG population)[14] and reported additional genetic variation flowering under LD conditions.[15]

Summary

Introduction

Common bean (Phaseolus vulgaris L.) has major significance as a staple food crop and source of dietary protein in many cultures around the world.[1]. Insight into the genetic basis of this variation is useful in tracing the history of common bean domestication, for guiding breeding efforts, and in gaining a better mechanistic understanding of photoperiod sensitivity and its evolution

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Discussion

Conclusion