The role of the FT genes in the control of flowering in chickpea

The transition from vegetative to reproductive stage is one of the most significant in the life cycle of any plant. Variation in flowering time allows species to colonize new habitats, and from an agricultural point of view is crucial to adapt crops to different environments and maximise yield. This is particularly important in the case of chickpea, which is cultivated in diverse environments in more than 50 countries. In most of these environments, early phenology plays a key role as an adaptation that allows the crop to escape unfavourable conditions. Therefore, flowering time is one of the most extensively studied traits in chickpea and numerous QTL studies have been published on this topic. FLOWERING LOCUS T (FT) is a key gene promoting flowering in Arabidopsis thaliana, and FT homologs are involved in the control of floral transition across plant kingdom, including legumes. This study investigated the putative role of CaFT homologues in the genetic control of flowering in chickpea. The molecular control of flowering time is well understood in model species, particularly Arabidopsis, which is the most suitable model for comparison with temperate legumes in view of its taxonomic position and nature of its flowering responses. This study explored the conservation and position of Arabidopsis flowering-related genes across chickpea genome, and discussed their co-localization with some reported flowering QTLs, focussing in particular on a central portion of chickpea chromosome 3 that has been recurrently associated with flowering in several mapping populations and published studies. The most plausible candidates in this region, belonged to the well-known CONSTANS-Like (COL) and FT gene families and these gene families were therefore characterised. Three different intra- and inter-specific chickpea populations were used in this study to investigate in more detail the possible identity of the genes underlying the co-localized flowering time QTLs on chromosome 3. QTL analysis and differential expression profiles in the three populations identified a cluster of three FT homologs (FTa1-FTa2-FTc) as the genes most likely to be responsible for the majority of the phenological difference between wild and cultivated chickpea. In contrast, in the intraspecific population, this locus has a lesser role that was secondary to a major locus in another region of chromosome 3. QTL analysis of shoot architecture traits revealed major loci controlling growth habit (erectness) and branching tendency between C. arietinum and C. reticulatum located in the same interval of chromosome 3, indicating a possible pleiotropic role of FT genes in control of shoot architecture. The growth habit QTL is likely equivalent to the previously-described growth habit locus Hg, suggesting that the FT cluster should be considered candidates for this locus. In view of their potential to influence chickpea phenology and thus its adaptation to different environments, sequence variation of the chickpea FTa1-FTa2-FTc cluster was examined in a panel of 96 accessions (94 C. arietinum and 2 C. reticulatum) through a targeted next-generation sequencing approach. This analysis showed that despite high conservation within the coding regions, the regulatory and intergenic regions are very divergent in the wild and domesticated species. Among domesticated accessions, the intergenic region between FTa1 and FTa2 shows the highest level of polymorphism, including the total deletion of the FTa2 gene and a 753 bp insertion that could be associated with variation in flowering time. Vernalization response has been a controversial topic in chickpea. Unlike C. reticulatum from which it derives, C. arietinum has been traditionally considered as a vernalization-insensitive species. However, more recent evidence points to the existence of two distinct vernalization response patterns within cultivated germplasm. This study evaluated the flowering phenotype of two wild and six cultivated chickpea accessions in response to vernalization and photoperiod, and the potential role of the chickpea FT homologs in these pathways was investigated through analysis of their expression patterns. The results indicate that a response to vernalization exists in all C. arietinum accessions, and suggest that the FTa1 gene may be particularly important in the signalling and integration of photoperiod and vernalization responses. The convergence of these two pathways on overlapping groups of FT genes may explain why a subset of chickpea accessions behave like they are vernalization insensitive under flowering-inductive photoperiods. Overall, the results obtained in the present study make a significant contribution to the current understanding of regulation of flowering time and growth habit in chickpea, including the molecular basis for a major flowering time locus and potential roles for FT homologues in the control of flowering time in both wild and domesticated chickpea