Plant trait heterosis is quantitatively associated with expression heterosis of the 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 of the leaf that may contribute to the known higher photosynthetic capacity of maize hybrids, we generated paired datasets of the proteomes and transcriptomes from leaf tissues of maize hybrids and their inbred parents. Expression patterns in the hybrids were semi-dominant to overdominant for subunits of the digenomic protein complexes required for the light reactions of photosynthesis and for chloroplast protein synthesis; nuclear and plastid-encoded subunits were elevated similarly. These patterns were not mirrored in the nuclear transcriptomes. We compared growth of multiple hybrids with varying levels of heterosis to transcript and protein levels. Expression heterosis (hybrid/mid-parent expression levels) of chloroplast ribosomal proteins and of nuclear transcripts for the photosynthetic light reactions was positively correlated with plant height heterosis (hybrid/mid-parent plant height). Ethylene biosynthetic enzymes were expressed below mid-parent levels in the hybrids, and the ethylene biosynthesis mutant acs2/acs6 partially phenocopied the hybrid proteome, indicating that a reduction in ethylene biosynthesis may be upstream of the elevated expression of photosynthetic and ribosomal proteins in chloroplasts of hybrids.

Heterosis in horticultural crop breeding: combining old theoretical bases with modern genomic views

“…In particular, similar to what emerged in cereals, such as maize (Yang et al, 2017;Liu et al, 2020a;Birdseye et al, 2021), rice (Dan et al, 2014;Shen et al, 2015;Zhu et al, 2016) and wheat (Song et al, 2009), multiple morphological features associated with vegetative tissue also showed different levels of heterosis in vegetable F1 hybrids. These insights, which have been observed depending on the crop and developmental stage, from post-germination to final yield, were derived from Brassicaceae crops, such as Chinese cabbage (Kawamura et al, 2016;Fujimoto et al, 2018;Shiraki et al, 2023), cabbage (Jeong et al, 2017), cauliflower (Verma and Kalia, 2017), rapeseed or canola (Brassica napus L.) (Basunanda et al, 2010;Wolko et al, 2019;Wang et al, 2021;Hu et al, 2022); Solanaceae crops, such as tomato (Chandel et al, 2021;Rajendran et al, 2022), potato (Buso et al, 2003), and eggplant (Kaushik, 2019;Kumar et al, 2020); Apiaceae crops, such as carrot, coriander and caraway (Jagosz, 2011;von Maydell et al, 2021;Hanifei et al, 2022); and Leguminosae crops, such as common bean (Goncalves-Vidigal et al, 2008) and pea (Sharma et al, 2023).…”

Triploid Hybrid Vigor in Above-Ground Growth and Methane Fermentation Efficiency of Energy Willow

“…In Table 3 , the MPH value (102.19%) was significant for the jasmonate isoleucine level in the TH3/12 plants. Presently, we lack an explanation for the detected jasmonic acid response in shoots of triploid willow hybrids, especially if we consider results from proteomic and transcriptomic analysis of seedling leaf tissues of the maize hybrid, B73xMo17, and its inbred parents ( Birdseye et al, 2021 ). These authors reported repression of jasmonic acid biosynthetic enzyme levels in that maize hybrid.…”

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

“…The proteome differences between chloroplasts of the hybrid and its inbred parents were not mirrored in their nuclear transcriptomes (SI Appendix, Fig. S4) (18,19). For example, most nuclear-encoded, plastid ribosomal subunit transcripts were higher in Mo17 than in B73 (SI Appendix, Fig.…”