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

['Saarah Kuzay', 'Department Of Plant Sciences', 'University Of California', 'Davis', 'California', 'United States Of America', 'Huiqiong Lin', 'Howard Hughes Medical Institute', 'Chevy Chase', 'Maryland']

Date: 2022-03

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. Results from this and our previous study 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 wheat varieties but is rare in durum wheat, where it might be particularly useful to improve grain yield.

A 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.

Funding: JD received support for this project from the Agriculture and Food Research Initiative Competitive Grants 2017-67007-25939 (WheatCAP), USDA National Institute of Food and Agriculture (NIFA, https://nifa.usda.gov/ ) and from the Howard Hughes Medical Institute ( https://www.hhmi.org/ ). The USDA-NIFA grant supported the salaries of SK, JZ and SC. The Howard Hughes Medical Institute supported the salaries of JD, HL, CL and DW. DW is a Howard Hughes Medical Institute Fellow of the Life Sciences Research Foundation ( http://www.lsrf.org/ ) that paid his salary for three years. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability: We deposited the Kronos near isogenic line with the H2 introgression in the National Small Grains Collection (PI 698810). All data are presented in the text and supplementary materials . The raw data for all figures and Supplemental Tables are available in S1 Data file.

Copyright: © 2022 Kuzay et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Our previous study established WAPO-A1 as the best candidate gene for the 7AL SNS QTL [ 10 ], but functional validation was missing. In this study, we demonstrate that WAPO1 is the gene underpinning the SNS QTL by characterizing loss-of-function mutants and transgenic plants and exploring its spatial and temporal distribution in the developing spike. We also describe the flower abnormalities observed in plants with complete loss of WAPO1 activity and in transgenic plants with additional WAPO1 genes. Finally, we characterize the effect of different natural WAPO-A1 alleles on the number of spikelets and grains per spike and discuss their potential applications in common and durum wheat breeding programs.

Rapid changes in WAPO-A1 allele frequencies during wheat domestication and breeding suggest that this region is relevant to wheat improvement [ 10 ]. Three major haplotypes were identified in the 87-kb candidate gene region–H1, H2, and H3 –each of which associated with different WAPO-A1 alleles. Haplotype H3 includes the ancestral alleles Wapo-A1c and Wapo-A1d, which differ from each other by two synonymous substitutions, two SNPs in the single intron and one in the promoter, which likely have limited effect on gene function [ 10 ]. Haplotype H3 is present in the diploid donor of the A genome (T. urartu), cultivated emmer (T. turgidum ssp. dicoccon) and wild emmer (T. turgidum ssp. dicoccoides), and at low frequency in modern durum and common wheat varieties. Haplotype H1, present in over 99% of modern durum wheat varieties, has the Wapo-A1a allele that is characterized by a 115-bp deletion in the promoter and a change from aspartic acid to asparagine at position 384 (D384N). This amino acid change is predicted to have a limited effect on protein structure and function ( Table 1 , BLOSUM62 score = 1). WAPO-A1 haplotype H2, the most frequent haplotype in modern common wheat varieties, carries the Wapo-A1b allele and differs from the ancestral haplotype by a cysteine to a phenylalanine polymorphism at amino acid position 47 (C47F) in a conserved region of the F-box motif [ 7 , 8 , 10 ]. This amino acid change is predicted to have a strong effect on protein structure and function ( Table 1 , BLOSUM62 score = -2). Linkage analysis in six different biparental populations established that the H2 haplotype was associated with higher SNS than both the H1 and H3 haplotypes [ 10 ].

In rice, mutations in APO1 or LFY (also known as APO2 and RFL in rice) result in reductions in the number of branches and spikelets per panicle. The effect is similar in the apo1 lfy double mutant, suggesting that these two genes act cooperatively to control this trait [ 15 ]. Mutations in these two genes are also associated with floral abnormalities, with more severe phenotypes in the apo1 lfy double mutant than in either of the two single mutants. These results suggest that these two genes also play important roles in floral development [ 15 ]. Floral defects in the rice apo1 and Arabidopsis ufo mutants are concentrated to the internal floral whorls [ 12 , 13 ].

The wheat gene TraesCS7A02G481600 is orthologous to the Oryza sativa (rice) gene ABERRANT PANICLE ORGANIZATION1 (APO1), hence it was designated as WHEAT ORTHOLOG of APO1 (WAPO1). Loss-of-function mutants in rice APO1 reduce panicle branching and spikelet number [ 11 ], supporting WAPO-A1 as a promising candidate gene for the SNS QTL [ 7 , 8 , 10 ]. The rice APO1 gene and its homolog in Arabidopsis thaliana (Arabidopsis), UNUSUAL FLORAL ORGANS (UFO), encode an F-box protein that is a component of an SCF ( S kp1– C ullin– F -box-protein) ubiquitin ligase [ 12 , 13 ]. This domain is important to maintain the activity of LEAFY (LFY), a transcription factor that plays key roles in flowering and floral development [ 14 ].

A highly significant and stable QTL for SNS was identified on chromosome arm 7AL in multiple genome-wide association studies (GWAS) including a panel of soft red winter wheats in the US [ 5 ], panels of European winter wheats [ 6 – 9 ], a panel of US and CIMMYT photoperiod-insensitive spring wheats, and six biparental populations which comprised different wheat market classes [ 10 ]. In our previous study, we generated two high-resolution genetic maps to delimit this SNS QTL to an 87-kb region (674,019,191–674,106,327 bp, RefSeq v1.1) containing four candidate genes [ 10 ]. Among these genes, we identified TraesCS7A02G481600 as the most promising candidate gene, based on the presence of a non-synonymous polymorphism that co-segregated with SNS in biparental populations segregating for different haplotypes in the candidate region [ 10 ].

Identifying genes controlling total grain yield is challenging due to its complex quantitative nature and genotype by environment interactions [ 3 ]. However, grain yield can be dissected into more discrete yield components with higher heritability. Total grain yield can be partitioned into several yield components, including number of spikes per area unit, spikelet number per spike (SNS), grain number per spikelet, and average grain weight. Among these traits, SNS usually exhibits high heritability because it is established early in the reproductive phase when the terminal spikelet is formed [ 4 ], limiting the effect of environmental conditions after this point.

Wheat is an essential staple crop for global food security. It is highly adapted to a wide variety of climates and production systems, and provides more than 20% of the calories and protein consumed by the human population [ 1 ]. Although further increases in grain yield are required to feed a continuously growing population, historical yield trend studies have shown a decrease in the relative rates of grain yield gains in some wheat growing regions [ 2 ]. This has prompted new efforts to understand and improve the productivity of both common (Triticum aestivum, genomes AABBDD) and durum wheat (T. turgidum ssp. durum, genomes AABB).

Results

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