Devon Birdseye, Laura A. de Boer, Hua Bai, Peng Zhou, Zhouxin Shen, Eric A. Schmelz, Nathan M. Springer, and Steven P. Briggs

PNAS November 23, 2021 118 (47) e2109332118

Significance

Heterosis (hybrid vigor) boosts the productivity and resilience of crops and livestock above the levels of both parents, yet its underlying mechanisms remain unknown. We analyzed expression patterns of proteins in maize hybrids and their inbred parents. Differences in several molecular machines and biochemical pathways were found and quantitatively assessed using a panel of 15 hybrids. Seedling leaf chloroplast ribosomal proteins were able to quantitatively infer levels of adult plant heterosis. Expression levels of biosynthetic enzymes for the stress hormone ethylene were reduced in hybrids, as was previously reported for the dicot Arabidopsis. Mutation of these genes in a maize inbred caused the proteome to resemble a hybrid. Repression of ethylene biosynthesis may be a conserved component of heterosis physiology.

Abstract

The use of hybrids is widespread in agriculture, yet the molecular basis for hybrid vigor (heterosis) remains obscure. To identify molecular components that may contribute to trait heterosis, we analyzed paired proteomic and transcriptomic data from seedling leaf and mature leaf blade tissues of maize hybrids and their inbred parents. Nuclear- and plastid-encoded subunits of complexes required for protein synthesis in the chloroplast and for the light reactions of photosynthesis were expressed above midparent and high-parent levels, respectively. Consistent with previous reports in Arabidopsis, ethylene biosynthetic enzymes were expressed below midparent levels in the hybrids, suggesting a conserved mechanism for heterosis between monocots and dicots. The ethylene biosynthesis mutant, acs2/acs6, largely phenocopied the hybrid proteome, indicating that a reduction in ethylene biosynthesis may mediate the differences between inbreds and their hybrids. To rank the relevance of expression differences to trait heterosis, we compared seedling leaf protein levels to the adult plant height of 15 hybrids. Hybrid/midparent expression ratios were most positively correlated with hybrid/midparent plant height ratios for the chloroplast ribosomal proteins. Our results show that increased expression of chloroplast ribosomal proteins in hybrid seedling leaves is mediated by reduced expression of ethylene biosynthetic enzymes and that the degree of their overexpression in seedlings can quantitatively predict adult trait heterosis.

See: https://www.pnas.org/content/118/47/e2109332118

Fig. 3. Density curves of Pearson correlations between protein expression heterosis and plant height heterosis in the combined RIL and six hybrids datasets.