Transcriptional signatures modulating shoot apical meristem morphometric and plant architectural traits enhance yield and productivity in chickpea

Abstract

Summary Plant height (PH) and plant width (PW), two of the major plant architectural traits determining the yield and productivity of a crop, are defined by diverse morphometric characteristics of the shoot apical meristem (SAM). The identification of potential molecular tags from a single gene that simultaneously modulates these plant/SAM architectural traits is therefore prerequisite to achieve enhanced yield and productivity in crop plants, including chickpea. Large‐scale multienvironment phenotyping of the association panel and mapping population have ascertained the efficacy of three vital SAM morphometric trait parameters, SAM width, SAM height and SAM area, as key indicators to unravel the genetic basis of the wide PW and PH trait variations observed in desi chickpea. This study integrated a genome‐wide association study (GWAS); quantitative trait locus (QTL)/fine‐mapping and map‐based cloning with molecular haplotyping; transcript profiling; and protein‐DNA interaction assays for the dissection of plant architectural traits in chickpea. These exertions delineated natural alleles and superior haplotypes from a CabHLH121 transcription factor (TF) gene within the major QTL governing PW, PH and SAM morphometric traits. A genome‐wide protein‐DNA interaction assay assured the direct binding of a known stem cell master regulator, CaWUS, to the WOX‐homeodomain TF binding sites of a CabHLH121 gene and its constituted haplotypes. The differential expression of CaWUS and transcriptional regulation of its target CabHLH121 gene/haplotypes were apparent, suggesting their collective role in altering SAM morphometric characteristics and plant architectural traits in the contrasting near isogenic lines (NILs). The NILs introgressed with a superior haplotype of a CabHLH121 exhibited optimal PW and desirable PH as well as enhanced yield and productivity without compromising any component of agronomic performance. These molecular signatures of the CabHLH121 TF gene have the potential to regulate both PW and PH traits through the modulation of proliferation, differentiation and maintenance of the meristematic stem cell population in the SAM; therefore, these signatures will be useful in the translational genomic study of chickpea genetic enhancement. The restructured cultivars with desirable PH (semidwarf) and PW will ensure maximal planting density in a specified cultivable field area, thereby enhancing the overall yield and productivity of chickpea. This can essentially facilitate the achievement of better remunerative outputs by farmers with rational land use, therefore ensuring global food security in the present scenario of an increasing population density and shrinking per capita land area.

CLAVATA signaling pathway genes modulating flowering time and flower number in chickpea

“…Deployment of SAM morphometric characteristics in QTL mapping will target master regulators influencing simultaneously a number of correlated agronomic traits 1 3 in crops. Correlation between SAM morphometrics and WUS gene expression in governing vital agromorphological traits is recently reported in chickpea (Narnoliya et al 2019). The differential expression analysis of the CaCLV3_01 gene and its haplotypes depicted a significant increase in its expression in early-flowering desi mapping parental accession, ICC 5590 and EDTF/HFN-NIL CaHAPA line as compared to its desi counterpart ICC 6306 and LDTF/LFN-NIL CaHAPB line.…”

“…The CLV signaling pathway is known to be associated with a number of agronomic traits such as inflorescence architecture, flower production and fruit size in tomato (Xu et al 2015). Recent studies reported the role of CLV-WUS signaling pathway-mediated stem cell regulation and related morpho-genes in modulation of the overall plant architecture (Whitewoods et al 2018;Narnoliya et al 2019). These aforesaid contextual collectively highlighted that the CLV genes are especially important SAM-mediated regulators of growth and development and thereby have potential to govern yield and architectural traits in multiple crop plants.…”

Restructuring plant types for developing tailor‐made crops

“…The axillary and inflorescence meristem, giving rise to leaves, branches and inflorescence, are derived from the SAM (Sharma and Fletcher, 2002; Yang and Jiao, 2016). The role of SAM morphometrics in regulating agronomic yield‐contributing traits is also known in crops like chickpea and maize (Basu et al ., 2019a; Leiboff et al ., 2015; Narnoliya et al ., 2019). The population of the meristematic cells is maintained through a feedback loop between the homeodomain transcription factor WUSCHEL (WUS) and its counterpart CLAVATA ( CLV ) gene family members and newly identified SQUAMOSA PROMOTER BINDING PROTEIN‐LIKE ( SPL ) family gene (Fouracre and Poethig, 2019; Somssich et al ., 2016).…”

“…Instead, it is maintained by the coordinate function of ABERRANT SPIKELET AND PANICLE1 (ASP1) and FLORAL ORGAN NUMBER2 (FON2; Suzuki et al ., 2019b). The CaWUS gene expression also regulates plant width in chickpea, where larger meristem size correlates with larger plant width (Narnoliya et al ., 2019). In tomato, allelic variants of WUS and CLV homologs control locule number and fruit size (Chu et al ., 2019; Muños et al ., 2011).…”

Auxin-regulated timing of transition from vegetative to reproductive growth in rapeseed (Brassica napus L.) under different nitrogen application rates

“…Appropriate timing of the transition from vegetative to reproductive growth is highly correlated with crop flowering time and yield (Narnoliya et al, 2019). The morphologic landmark of this change is a protrusion in the peripheral zone, which is called flower primordium (Carles and Fletcher, 2003).…”