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

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 mai...

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Autores principales: Birdseye, Devon, de Boer, Laura A., Bai, Hua, Zhou, Peng, Shen, Zhouxin, Schmelz, Eric A., Springer, Nathan M., Briggs, Steven P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8617506/
https://www.ncbi.nlm.nih.gov/pubmed/34782463
http://dx.doi.org/10.1073/pnas.2109332118
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author Birdseye, Devon
de Boer, Laura A.
Bai, Hua
Zhou, Peng
Shen, Zhouxin
Schmelz, Eric A.
Springer, Nathan M.
Briggs, Steven P.
author_facet Birdseye, Devon
de Boer, Laura A.
Bai, Hua
Zhou, Peng
Shen, Zhouxin
Schmelz, Eric A.
Springer, Nathan M.
Briggs, Steven P.
author_sort Birdseye, Devon
collection PubMed
description 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.
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spelling pubmed-86175062021-12-09 Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins Birdseye, Devon de Boer, Laura A. Bai, Hua Zhou, Peng Shen, Zhouxin Schmelz, Eric A. Springer, Nathan M. Briggs, Steven P. Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2021-11-15 2021-11-23 /pmc/articles/PMC8617506/ /pubmed/34782463 http://dx.doi.org/10.1073/pnas.2109332118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Birdseye, Devon
de Boer, Laura A.
Bai, Hua
Zhou, Peng
Shen, Zhouxin
Schmelz, Eric A.
Springer, Nathan M.
Briggs, Steven P.
Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins
title Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins
title_full Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins
title_fullStr Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins
title_full_unstemmed Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins
title_short Plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins
title_sort plant height heterosis is quantitatively associated with expression levels of plastid ribosomal proteins
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8617506/
https://www.ncbi.nlm.nih.gov/pubmed/34782463
http://dx.doi.org/10.1073/pnas.2109332118
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