Genome-Wide Characterization of Ascorbate Peroxidase Gene Family in Peanut (Arachis hypogea L.) Revealed Their Crucial Role in Growth and Multiple Stress Tolerance

Ascorbate peroxidase (APX), an important antioxidant enzyme, plays a significant role in ROS scavenging by catalyzing the decrease of hydrogen peroxide under various environmental stresses. Nevertheless, information about the APX gene family and their evolutionary and functional attributes in peanut...

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Main Authors: Ali Raza, Yasir Sharif, Kun Chen, Lihui Wang, Huiwen Fu, Yuhui Zhuang, Annapurna Chitikineni, Hua Chen, Chong Zhang, Rajeev K. Varshney, Weijian Zhuang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.962182/full
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author Ali Raza
Yasir Sharif
Kun Chen
Lihui Wang
Huiwen Fu
Yuhui Zhuang
Annapurna Chitikineni
Hua Chen
Hua Chen
Chong Zhang
Chong Zhang
Rajeev K. Varshney
Rajeev K. Varshney
Weijian Zhuang
Weijian Zhuang
author_facet Ali Raza
Yasir Sharif
Kun Chen
Lihui Wang
Huiwen Fu
Yuhui Zhuang
Annapurna Chitikineni
Hua Chen
Hua Chen
Chong Zhang
Chong Zhang
Rajeev K. Varshney
Rajeev K. Varshney
Weijian Zhuang
Weijian Zhuang
author_sort Ali Raza
collection DOAJ
description Ascorbate peroxidase (APX), an important antioxidant enzyme, plays a significant role in ROS scavenging by catalyzing the decrease of hydrogen peroxide under various environmental stresses. Nevertheless, information about the APX gene family and their evolutionary and functional attributes in peanut (Arachis hypogea L.) was not reported. Therefore, a comprehensive genome-wide study was performed to discover the APX genes in cultivated peanut genome. This study identified 166 AhAPX genes in the peanut genome, classified into 11 main groups. The gene duplication analysis showed that AhAPX genes had experienced segmental duplications and purifying selection pressure. Gene structure and motif investigation indicated that most of the AhAPX genes exhibited a comparatively well-preserved exon-intron pattern and motif configuration contained by the identical group. We discovered five phytohormones-, six abiotic stress-, and five growth and development-related cis-elements in the promoter regions of AhAPX. Fourteen putative ah-miRNAs from 12 families were identified, targeting 33 AhAPX genes. Furthermore, we identified 3,257 transcription factors from 38 families (including AP2, ARF, B3, bHLH, bZIP, ERF, MYB, NAC, WRKY, etc.) in 162 AhAPX genes. Gene ontology and KEGG enrichment analysis confirm the role of AhAPX genes in oxidoreductase activity, catalytic activity, cell junction, cellular response to stimulus and detoxification, biosynthesis of metabolites, and phenylpropanoid metabolism. Based on transcriptome datasets, some genes such as AhAPX4/7/17/77/82/86/130/133 and AhAPX160 showed significantly higher expression in diverse tissues/organs, i.e., flower, leaf, stem, roots, peg, testa, and cotyledon. Likewise, only a few genes, including AhAPX4/17/19/55/59/82/101/102/137 and AhAPX140, were significantly upregulated under abiotic (drought and cold), and phytohormones (ethylene, abscisic acid, paclobutrazol, brassinolide, and salicylic acid) treatments. qRT-PCR-based expression profiling presented the parallel expression trends as generated from transcriptome datasets. Our discoveries gave new visions into the evolution of APX genes and provided a base for further functional examinations of the AhAPX genes in peanut breeding programs.
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spelling doaj.art-da724b2b53d84195b758aacdec8ca6ef2022-12-22T02:03:43ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-09-011310.3389/fpls.2022.962182962182Genome-Wide Characterization of Ascorbate Peroxidase Gene Family in Peanut (Arachis hypogea L.) Revealed Their Crucial Role in Growth and Multiple Stress ToleranceAli Raza0Yasir Sharif1Kun Chen2Lihui Wang3Huiwen Fu4Yuhui Zhuang5Annapurna Chitikineni6Hua Chen7Hua Chen8Chong Zhang9Chong Zhang10Rajeev K. Varshney11Rajeev K. Varshney12Weijian Zhuang13Weijian Zhuang14Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Center of Legume Plant Genetics and Systems Biology, College of Agriculture, Oil Crops Research Institute, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCollege of Plant Protection, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCollege of Plant Protection, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCollege of Plant Protection, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCollege of Plant Protection, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCollege of Life Science, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaMurdoch’s Centre for Crop and Food Innovation, State Agricultural Biotechnology Centre, Food Futures Institute, Murdoch University, Murdoch, WA, AustraliaKey Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Center of Legume Plant Genetics and Systems Biology, College of Agriculture, Oil Crops Research Institute, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCollege of Plant Protection, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaKey Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Center of Legume Plant Genetics and Systems Biology, College of Agriculture, Oil Crops Research Institute, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCollege of Plant Protection, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaKey Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Center of Legume Plant Genetics and Systems Biology, College of Agriculture, Oil Crops Research Institute, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaMurdoch’s Centre for Crop and Food Innovation, State Agricultural Biotechnology Centre, Food Futures Institute, Murdoch University, Murdoch, WA, AustraliaKey Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Center of Legume Plant Genetics and Systems Biology, College of Agriculture, Oil Crops Research Institute, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaCollege of Plant Protection, Fujian Agriculture and Forestry University (FAFU), Fuzhou, ChinaAscorbate peroxidase (APX), an important antioxidant enzyme, plays a significant role in ROS scavenging by catalyzing the decrease of hydrogen peroxide under various environmental stresses. Nevertheless, information about the APX gene family and their evolutionary and functional attributes in peanut (Arachis hypogea L.) was not reported. Therefore, a comprehensive genome-wide study was performed to discover the APX genes in cultivated peanut genome. This study identified 166 AhAPX genes in the peanut genome, classified into 11 main groups. The gene duplication analysis showed that AhAPX genes had experienced segmental duplications and purifying selection pressure. Gene structure and motif investigation indicated that most of the AhAPX genes exhibited a comparatively well-preserved exon-intron pattern and motif configuration contained by the identical group. We discovered five phytohormones-, six abiotic stress-, and five growth and development-related cis-elements in the promoter regions of AhAPX. Fourteen putative ah-miRNAs from 12 families were identified, targeting 33 AhAPX genes. Furthermore, we identified 3,257 transcription factors from 38 families (including AP2, ARF, B3, bHLH, bZIP, ERF, MYB, NAC, WRKY, etc.) in 162 AhAPX genes. Gene ontology and KEGG enrichment analysis confirm the role of AhAPX genes in oxidoreductase activity, catalytic activity, cell junction, cellular response to stimulus and detoxification, biosynthesis of metabolites, and phenylpropanoid metabolism. Based on transcriptome datasets, some genes such as AhAPX4/7/17/77/82/86/130/133 and AhAPX160 showed significantly higher expression in diverse tissues/organs, i.e., flower, leaf, stem, roots, peg, testa, and cotyledon. Likewise, only a few genes, including AhAPX4/17/19/55/59/82/101/102/137 and AhAPX140, were significantly upregulated under abiotic (drought and cold), and phytohormones (ethylene, abscisic acid, paclobutrazol, brassinolide, and salicylic acid) treatments. qRT-PCR-based expression profiling presented the parallel expression trends as generated from transcriptome datasets. Our discoveries gave new visions into the evolution of APX genes and provided a base for further functional examinations of the AhAPX genes in peanut breeding programs.https://www.frontiersin.org/articles/10.3389/fpls.2022.962182/fullabiotic stressantioxidantdroughtgenomicsgene ontologylegume
spellingShingle Ali Raza
Yasir Sharif
Kun Chen
Lihui Wang
Huiwen Fu
Yuhui Zhuang
Annapurna Chitikineni
Hua Chen
Hua Chen
Chong Zhang
Chong Zhang
Rajeev K. Varshney
Rajeev K. Varshney
Weijian Zhuang
Weijian Zhuang
Genome-Wide Characterization of Ascorbate Peroxidase Gene Family in Peanut (Arachis hypogea L.) Revealed Their Crucial Role in Growth and Multiple Stress Tolerance
Frontiers in Plant Science
abiotic stress
antioxidant
drought
genomics
gene ontology
legume
title Genome-Wide Characterization of Ascorbate Peroxidase Gene Family in Peanut (Arachis hypogea L.) Revealed Their Crucial Role in Growth and Multiple Stress Tolerance
title_full Genome-Wide Characterization of Ascorbate Peroxidase Gene Family in Peanut (Arachis hypogea L.) Revealed Their Crucial Role in Growth and Multiple Stress Tolerance
title_fullStr Genome-Wide Characterization of Ascorbate Peroxidase Gene Family in Peanut (Arachis hypogea L.) Revealed Their Crucial Role in Growth and Multiple Stress Tolerance
title_full_unstemmed Genome-Wide Characterization of Ascorbate Peroxidase Gene Family in Peanut (Arachis hypogea L.) Revealed Their Crucial Role in Growth and Multiple Stress Tolerance
title_short Genome-Wide Characterization of Ascorbate Peroxidase Gene Family in Peanut (Arachis hypogea L.) Revealed Their Crucial Role in Growth and Multiple Stress Tolerance
title_sort genome wide characterization of ascorbate peroxidase gene family in peanut arachis hypogea l revealed their crucial role in growth and multiple stress tolerance
topic abiotic stress
antioxidant
drought
genomics
gene ontology
legume
url https://www.frontiersin.org/articles/10.3389/fpls.2022.962182/full
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