Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins

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.

HybridExpress: an R/Bioconductor package for comparative transcriptomic analyses of hybrids and their progenitors

“…Changes in gene expression have been linked to heterosis in many plant traits, such as seed germination and plant height in maize (Birdseye et al ., 2021; Wan et al ., 2022), yield in rice (Sun et al ., 2023), and nicotine biosynthesis in Nicotiana tabacum (Tian et al ., 2018). However, such changes in transcriptional programs can (and possibly will) vary in a spatiotemporal scale, resulting in tissue- or condition-specific changes in the strength of heterosis (Ko et al ., 2016; Yang et al ., 2021).…”

Striking a growth–defense balance: Stress regulators that function in maize development

“…Arabidopsis hybrids exhibited significantly lower levels of ET biosynthesis than the mid‐parent levels, and their biomass vigor diminished in response to exogenous ET treatment and increasing endogenous ET production (Song et al, 2018). Similarly, the expression levels of ET biosynthetic genes in maize hybrids were lower than the mid‐parent levels, and the proteome of the ET biosynthetic mutant Zmacs2 Zmacs6 phenocopied that of the hybrid to a large extent (Birdseye et al, 2021). Furthermore, recent research has demonstrated that the ET biosynthetic gene ZmACO2 and ARGOS1 (encoding a negative regulator of ET sensitivity) are heterosis‐associated genes whose structural variations contribute to maize yield heterosis in an overdominance fashion (Guo et al, 2014; Wang et al, 2023).…”

Protein nonadditive expression and solubility inArabidopsishybrids and allotetraploids

“…In maize hybrids, metabolic changes correspond to nonadditive protein abundance and enzyme activities of key enzymes in the respective pathways, suggesting that concerted changes in metabolomes and proteomes contribute to maize heterosis (LI et al 2020). Another study indicates increased expression of nuclear-and plastid-encoded subunits of protein complexes required for protein synthesis in chloroplasts and for photosynthetic activities in hybrid seedling leaves, and hybrid/mid-parent expression ratios of chloroplast ribosomal proteins are correlated with plant height heterosis (BIRDSEYE et al 2021). These results suggest that post-transcriptional regulation and protein synthesis play a role in regulating the nonadditive expression of proteins in hybrids (NG et al 2012;YANG et al 2021).…”

“…2020). Another study indicates increased expression of nuclear- and plastid-encoded subunits of protein complexes required for protein synthesis in chloroplasts and for photosynthetic activities in hybrid seedling leaves, and hybrid/mid-parent expression ratios of chloroplast ribosomal proteins are correlated with plant height heterosis (B irdseye et al . 2021).…”