WAPO-A1 is the causal gene of the 7AL QTL for spikelet number per spike in wheat

Abstract

Improving our understanding of the genes regulating grain yield can contribute to the development of more productive wheat varieties. Previously, a highly significant QTL affecting spikelet number per spike (SNS), grain number per spike (GNS) and grain yield was detected on chromosome arm 7AL in multiple genome-wide association studies. Using a high-resolution genetic map, we established that the A-genome homeolog of WHEAT ORTHOLOG OF APO1 (WAPO-A1) was a leading candidate gene for this QTL. Using mutants and transgenic plants, we demonstrate in this study that WAPO-A1 is the causal gene underpinning this QTL. Loss-of-function mutants wapo-A1 and wapo-B1 showed reduced SNS in tetraploid wheat, and the effect was exacerbated in wapo1 combining both mutations. By contrast, spikes of transgenic wheat plants carrying extra copies of WAPO-A1 driven by its native promoter had higher SNS, a more compact spike apical region and a smaller terminal spikelet than the wild type. Taken together, these results indicate that WAPO1 affects SNS by regulating the timing of terminal spikelet formation. Both transgenic and wapo1 mutant plants showed a wide range of floral abnormalities, indicating additional roles of WAPO1 on wheat floral development. Previously, we found three widespread haplotypes in the QTL region (H1, H2 and H3), each associated with particular WAPO-A1 alleles. Integrating results from this study and previous findings, we show that the WAPO-A1 allele in the H1 haplotype (115-bp deletion in the promoter) is expressed at significantly lower levels in the developing spikes than the alleles in the H2 and H3 haplotypes, resulting in reduced SNS. Field experiments also showed that the H2 haplotype is associated with the strongest effects in increasing SNS and GNS (H2>H3>H1). The H2 haplotype is already present in most modern common wheats, so it might be particularly useful in durum wheat where H2 is rare. AUTHOR SUMMARYA region on wheat chromosome 7A has been previously shown to affect the number of spikelets and grains per spike as well as total grain yield in multiple breeding programs. In this study, we show that loss-of-function mutations in the WAPO1 gene located within this region reduce the number of spikelets per spike and that additional transgenic copies of this gene increase this number. These results demonstrate that WAPO1 is the gene responsible for the differences in grain number and yield associated with the 7A chromosome region. Among the three main variants identified for this gene, we demonstrate in field experiments that the H2 variant is associated with the largest increases in number of spikelets and grains per spike. The H2 WAPO1 variant is frequent in bread wheat breeding programs but is almost absent in modern pasta wheat varieties. Therefore, the introgression of the H2 represents a promising opportunity to improve grain yield in pasta wheat breeding programs.