Chinese scientists find structural variation that boosts grain number in sorghum

Chinese scientists have uncovered two major genes responsible for sorghum's double-grain spikelet, which dramatically enhance grain number and crop yield. A substantial 35.7-kilobase intrachromosomal inversion at the DG1 (Double-Grain 1) promoter drives the upregulation of DG1 expression, leading to the development of double-grain spikelets that remarkably increase sorghum grain number while illustrating the critical role of genomic structural variation in plant evolution.

This study, published in Nature Plants, was conducted by Prof. XIE Qi's team at the Institute of Genetics and Developmental Biology (IGDB) of the Chinese Academy of Sciences, in collaboration with five other institutions.

Sorghum, a staple grain crop, typically produces a single seed per spikelet, with the lower floret in each spikelet aborting during development. However, certain sorghum varieties exhibit a double-grain spikelet trait, wherein both florets develop seeds, with a significant boost in grain yield. The phenomenon of multiple-seeded spikelets is common in gramineous crops, such as grasses and bamboo, and has long intrigued researchers. As early as 1936, Karper and Stephens reported that sorghum's double-grain spikelet trait could increase grain number by over 50%, though its genetic basis remained unknown for nearly a century.

By constructing three genetically segregated populations, the researchers mapped the dominant locus for double-grain spikelets to a 49.5-kilobase interval. They identified a 35.7-kilobase chromosomal inversion in this region that enhanced the expression of ORF1 while reducing the expression of ORF5. Functional analyses confirmed that increased ORF1 expression triggered the double-grain spikelet phenotype, whereas knocking out ORF5 had no effect. Consequently, ORF1 was designated DG1. This gene encodes a homeobox-domain protein homologous to WUSCHEL (WUS) proteins found in Arabidopsis thaliana, maize, and rice.

Further analysis revealed that the inversion at the DG1 promoter significantly reduced the repressive histone methylation marks H3K27me3 and H3K9me2, alleviating transcriptional repression and enhancing DG1 expression.

In the young panicle stage, compared with single-grain spikelets in which the lower floret degenerates, double-grain spikelets maintain visible lower floret meristems at the young panicle stage. During flowering, single-grain spikelets produce only one fertile upper floret, while double-grain spikelets develop two complete pistils and four to six stamens. This suggests that DG1 regulates floret meristem formation and differentiation, restoring the fertility of the lower floret and leading to the double-grain trait.

Field trials conducted in Beijing and Shenzhen over multiple years demonstrated that DG1 has no negative impact on key agronomic traits such as plant height, tillering, or flowering time. Although plants carrying the DG1 allele showed a slight decrease in thousand-grain weight, they exhibited a 40.7% to 46.1% increase in grain number per panicle, an 8.6% to 12.4% rise in grain weight per panicle, and a 10.1% to 14.3% boost in overall yield per plot. These results suggest that DG1 is a valuable genetic resource for breeding high-yield sorghum through molecular design.

In conclusion, this study cloned the DG1 gene that controls the double-grain spikelet trait in sorghum, revealed the key mechanism by which the genomic structural variation of DG1 controls the fertility of the lower florets of sorghum spikelets, and discovered a new path to increase the number of grains per panicle and the yield of crops.

It is worth noting that large brewing enterprises in China, such as Kweichow Moutai and Wuliangye, which are in the Chishui River Basin, use sorghum varieties with small grains as well as resistance to boiling and gelatinization as raw materials. Grains associated with DG1 are smaller, with an increased specific surface area, and their resistance to boiling is significantly improved. Moreover, the number of grains per panicle and yield are higher.

Therefore, it is an excellent gene resource for the molecular design of sorghum varieties used for brewing. It is expected that this achievement will contribute to the production of raw grains for China's brewing industry.