Genome-wide identification and comparative analyses of key genes involved in C4 photosynthesis in five main gramineous crops

Compared to C3 species, C4 plants showed higher photosynthetic capacity as well as water and nitrogen use efficiency due to the presence of the C4 photosynthetic pathway. Previous studies have shown that all genes required for the C4 photosynthetic pathway exist in the genomes of C3 species and are...

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Main Authors: Liang Chen, Yang Yang, Zhangchen Zhao, Shan Lu, Qiumei Lu, Chunge Cui, Martin A. J. Parry, Yin-Gang Hu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1134170/full
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author Liang Chen
Yang Yang
Zhangchen Zhao
Shan Lu
Qiumei Lu
Chunge Cui
Martin A. J. Parry
Yin-Gang Hu
Yin-Gang Hu
author_facet Liang Chen
Yang Yang
Zhangchen Zhao
Shan Lu
Qiumei Lu
Chunge Cui
Martin A. J. Parry
Yin-Gang Hu
Yin-Gang Hu
author_sort Liang Chen
collection DOAJ
description Compared to C3 species, C4 plants showed higher photosynthetic capacity as well as water and nitrogen use efficiency due to the presence of the C4 photosynthetic pathway. Previous studies have shown that all genes required for the C4 photosynthetic pathway exist in the genomes of C3 species and are expressed. In this study, the genes encoding six key C4 photosynthetic pathway enzymes (β-CA, PEPC, ME, MDH, RbcS, and PPDK) in the genomes of five important gramineous crops (C4: maize, foxtail millet, and sorghum; C3: rice and wheat) were systematically identified and compared. Based on sequence characteristics and evolutionary relationships, their C4 functional gene copies were distinguished from non-photosynthetic functional gene copies. Furthermore, multiple sequence alignment revealed important sites affecting the activities of PEPC and RbcS between the C3 and C4 species. Comparisons of expression characteristics confirmed that the expression patterns of non-photosynthetic gene copies were relatively conserved among species, while C4 gene copies in C4 species acquired new tissue expression patterns during evolution. Additionally, multiple sequence features that may affect C4 gene expression and subcellular localization were found in the coding and promoter regions. Our work emphasized the diversity of the evolution of different genes in the C4 photosynthetic pathway and confirmed that the specific high expression in the leaf and appropriate intracellular distribution were the keys to the evolution of C4 photosynthesis. The results of this study will help determine the evolutionary mechanism of the C4 photosynthetic pathway in Gramineae and provide references for the transformation of C4 photosynthetic pathways in wheat, rice, and other major C3 cereal crops.
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spelling doaj.art-832592cb1f8346caa6d00eefbf2f67592023-03-13T05:15:45ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-03-011410.3389/fpls.2023.11341701134170Genome-wide identification and comparative analyses of key genes involved in C4 photosynthesis in five main gramineous cropsLiang Chen0Yang Yang1Zhangchen Zhao2Shan Lu3Qiumei Lu4Chunge Cui5Martin A. J. Parry6Yin-Gang Hu7Yin-Gang Hu8State Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, Shaanxi, ChinaCollege of Agriculture, Shannxi Agricultural University (Institute of Crop Sciences), Taiyuan, Shanxi, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, Shaanxi, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, Shaanxi, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, Shaanxi, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, Shaanxi, ChinaLancaster Environment Centre, Lancaster University, Lancaster, United KingdomState Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, Shaanxi, ChinaInstitute of Water Saving Agriculture in Arid Regions of China, Northwest A&F University, Yangling, Shaanxi, ChinaCompared to C3 species, C4 plants showed higher photosynthetic capacity as well as water and nitrogen use efficiency due to the presence of the C4 photosynthetic pathway. Previous studies have shown that all genes required for the C4 photosynthetic pathway exist in the genomes of C3 species and are expressed. In this study, the genes encoding six key C4 photosynthetic pathway enzymes (β-CA, PEPC, ME, MDH, RbcS, and PPDK) in the genomes of five important gramineous crops (C4: maize, foxtail millet, and sorghum; C3: rice and wheat) were systematically identified and compared. Based on sequence characteristics and evolutionary relationships, their C4 functional gene copies were distinguished from non-photosynthetic functional gene copies. Furthermore, multiple sequence alignment revealed important sites affecting the activities of PEPC and RbcS between the C3 and C4 species. Comparisons of expression characteristics confirmed that the expression patterns of non-photosynthetic gene copies were relatively conserved among species, while C4 gene copies in C4 species acquired new tissue expression patterns during evolution. Additionally, multiple sequence features that may affect C4 gene expression and subcellular localization were found in the coding and promoter regions. Our work emphasized the diversity of the evolution of different genes in the C4 photosynthetic pathway and confirmed that the specific high expression in the leaf and appropriate intracellular distribution were the keys to the evolution of C4 photosynthesis. The results of this study will help determine the evolutionary mechanism of the C4 photosynthetic pathway in Gramineae and provide references for the transformation of C4 photosynthetic pathways in wheat, rice, and other major C3 cereal crops.https://www.frontiersin.org/articles/10.3389/fpls.2023.1134170/fullGramineae cropsC4 photosynthesisC3 photosynthesisPhylogenetic analysisExpression pattern
spellingShingle Liang Chen
Yang Yang
Zhangchen Zhao
Shan Lu
Qiumei Lu
Chunge Cui
Martin A. J. Parry
Yin-Gang Hu
Yin-Gang Hu
Genome-wide identification and comparative analyses of key genes involved in C4 photosynthesis in five main gramineous crops
Frontiers in Plant Science
Gramineae crops
C4 photosynthesis
C3 photosynthesis
Phylogenetic analysis
Expression pattern
title Genome-wide identification and comparative analyses of key genes involved in C4 photosynthesis in five main gramineous crops
title_full Genome-wide identification and comparative analyses of key genes involved in C4 photosynthesis in five main gramineous crops
title_fullStr Genome-wide identification and comparative analyses of key genes involved in C4 photosynthesis in five main gramineous crops
title_full_unstemmed Genome-wide identification and comparative analyses of key genes involved in C4 photosynthesis in five main gramineous crops
title_short Genome-wide identification and comparative analyses of key genes involved in C4 photosynthesis in five main gramineous crops
title_sort genome wide identification and comparative analyses of key genes involved in c4 photosynthesis in five main gramineous crops
topic Gramineae crops
C4 photosynthesis
C3 photosynthesis
Phylogenetic analysis
Expression pattern
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1134170/full
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