Maize team at Huazhong Agricultural University develops a new key to exploit the advantages of maize hybrids through interdisciplinary collaboration

Maize is one of the world's largest food and feed crops, with global production exceeding 1 billion tons per year. Maize was also one of the first crops in the world to utilize hybrid advantage and one of the most thoroughly utilized. In the last hundred years, a large number of researchers have conducted extensive research on hybrid advantage in crops such as rice, maize and oilseed rape. However, these studies are often based on a single genetic population, and there are limitations to the understanding of heterosis.

Our maize research team has constructed a maize synthetic CUBIC population with 24 maize backbone materials commonly used in breeding in China in the early stage and exhausted ten years of work. On this basis, to systematically analyze maize hybrid advantage, the team created the largest set of hybrid genetic design populations in plants to date, with a total of 42,820 F1 hybrids covering 30 groups of semi-sibling F1 populations. This F1 population has a wide diversity and a clear genetic background, which is ideal for studying heterosis and provides excellent intermediate material for maize genetic breeding. 2017, with the support of Anhui Fengda Seed Company, the team of Prof. Jianbing Yan and Prof. Lu Zhi from Tsinghua University jointly launched the Maize Heterosis Prediction Challenge (e-Maize Challenge), looking forward to Through the Challenge, a precise, robust and efficient computational analysis method was established using the provided genomics data and the innovative data analysis methods of the participants to achieve the accurate prediction of hybrid combinations with strong dominant phenotypes using genomics big data. More than 30 teams from different disciplines and industries, including universities and companies from all over the world, competed in the competition, and Professor Wang Xiangfeng's team from China Agricultural University finally won the championship.

On the basis of the challenge, all parties further cooperated deeply to explore the organic integration of basic, application and development. After years of research, the team combined genomic big data, machine learning and genome-wide association analysis methods to systematically analyze the genetic basis of maize hybrid advantage and special cooperativity formation in 42,820 F1 hybrids, and discovered a "dominant-mutual" co-regulatory model with important contribution to the formation of hybrid advantage. The study revealed that a "dominant-mutual" co-regulatory model makes an important contribution to the formation of hybrid advantage. Through crosses, dominant complementation broadly disengaged genomic repressive interactions in the parents and activated the expression of repressed master loci in the parents, resulting in heterozygous dominance in maize F1. Several predicted F1 combinations based on these genomically designed hybrid combinations have entered the district test and release phase.

The results were published in Genome Biology on May 10, 2021 under the title "The genetic mechanism of heterosis utilization in maizeimprovement". The genetic mechanism of heterosis utilization in maizeimprovement" was published in Genome Biology (Genome Biology). Associate Professor Xiao Yingjie from the School of Plant Science and Technology, Postdoctoral Fellow Jiang Shuqin from China Agricultural University, PhD student Cheng Qian from Northwest Agriculture and Forestry University, and Dr. Wang Xiaqing from Beijing Academy of Agricultural and Forestry Sciences were the co-first authors of the paper. Professor Jianbing Yan, Professor Xiangfeng Wang from China Agricultural University and Researcher Jiuran Zhao from Beijing Academy of Agricultural and Forestry Sciences were the co-corresponding authors.

According to the researchers, the mathematical modeling to identify genes for heterozygous dominance and find the optimal combination of genes for trait improvement, as well as the use of gene editing technology to create superior variants, is expected to accurately select one in a thousand or one in ten thousand breeding materials, which will greatly reduce breeding costs and accelerate the breeding process.

In maize hybrid breeding, complementary pools of parental lines with reshuffled genetic variants are established for superior hybrid performance. To comprehensively decipher the genetics of heterosis, we present a new design of multiple linked F1 populations with 42,840 F1 maize hybrids, generated by crossing a synthetic population of 1428 maternal lines with 30 elite testers from diverse genetic backgrounds and phenotyped for agronomic traits.

We show that, although yield heterosis is correlated with the widespread, minor-effect epistatic QTLs, it may be resulted from a few major-effect additive and dominant QTLs in early developmental stages. Floral transition is probably one critical stage for heterosis formation, in which epistatic QTLs are activated by paternal contributions of alleles that counteract the recessive, deleterious maternal alleles. These deleterious alleles, while rare, epistatically repress other favorable QTLs. We demonstrate this with one example, showing that Brachytic2 represses the Ubiquitin3 locus in the maternal lines; in hybrids, the paternal allele alleviates this repression, which in turn recovers the height of the plant and enhances the weight of the ear. Finally, we propose a molecular design breeding by manipulating key genes underlying the transition from vegetative-to-reproductive growth.

The new population design is used to dissect the genetic basis of heterosis which accelerates maize molecular design breeding by diminishing deleterious epistatic interactions.