A systematic dissection in oilseed rape provides insights into the genetic architecture and molecular mechanism of yield heterosis

Abstract

Summary Heterosis refers to the better performance of cross progeny compared with inbred parents, and its utilization contributes greatly to agricultural production. Several hypotheses have been proposed to explain heterosis mainly including dominance, over‐dominance (or pseudo‐overdominance) and epistasis. However, systematic dissection and verification of these hypotheses are rarely documented. Here, comparison of heterosis level across different traits showed that the strong heterosis of composite traits (such as yield) could be attributed to the multiplicative effects of moderate heterosis of component traits, whether at the genome or locus level. Yield heterosis was regulated by a complex trait‐QTL network that was characterized by obvious centre‐periphery structure, hub QTL, complex up/downstream and positive/negative feedback relationships. More importantly, we showed that better‐parent heterosis on yield could be produced in a cross of two near‐isogenic lines by the pyramiding and complementation of two major heterotic QTL showing partial‐dominance on yield components. The causal gene (BnaA9.CYP78A9) of QC14 was identified, and its heterotic effect results from the heterozygous status of a CACTA‐like transposable element in its upstream regulatory region, which led to partial dominance at expression and auxin levels, thus resulting in non‐additive expression of downstream responsive genes involved in cell cycle and proliferation, eventually leading to the heterosis of cell number. Taken together, the results at the phenotypic, genetic and molecular levels were highly consistent, which demonstrated that the pyramiding effect of heterotic QTL and the multiplicative effect of individual component traits could well explain substantial parts of yield heterosis in oilseed rape. These results provide in‐depth insights into the genetic architecture and molecular mechanism of yield heterosis.

Toward understanding and utilizing crop heterosis in the age of biotechnology

“… 11 In maize, through a design of multiple linked F 1 populations containing 42,840 F 1 hybrids and genome-wide association study, an instance of epistasis was revealed where one recessive, deleterious maternal allele, Brachytic2 , repressed the favorable Ubiquitin3 locus in the maternal lines, while the paternal allele alleviated this repression and thus recovered plant height and ear weight in hybrids. 10 The genomic architectures of heterosis in rice, maize, wheat, and other crops were also characterized using the population-based method, 6 , 7 , 12 , 13 , 26 , 27 , 44 which uncovered many novel loci functioning in heterosis via dominance, overdominance, and epistasis. These loci were dynamically predominant for different heterotic traits during plant life cycle and could serve as important references for genotype-based parent selection in hybrid breeding ( Figure 1 B).…”