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

Ali Raza; Yasir Sharif; Kun Chen; Lihui Wang; Huiwen Fu; Yuhui Zhuang; Annapurna Chitikineni; Hua Chen; Chong Zhang; Rajeev K Varshney; Weijian Zhuang

doi:10.3389/fpls.2022.962182

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

Front Plant Sci. 2022 Sep 9:13:962182. doi: 10.3389/fpls.2022.962182. eCollection 2022.

Authors

Ali Raza¹, Yasir Sharif², Kun Chen², Lihui Wang², Huiwen Fu², Yuhui Zhuang³, Annapurna Chitikineni⁴, Hua Chen^{1

2}, Chong Zhang^{1

2}, Rajeev K Varshney^{1

4}, Weijian Zhuang^{1

2}

Affiliations

¹ Key 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, China.
² College of Plant Protection, Fujian Agriculture and Forestry University (FAFU), Fuzhou, China.
³ College of Life Science, Fujian Agriculture and Forestry University (FAFU), Fuzhou, China.
⁴ Murdoch's Centre for Crop and Food Innovation, State Agricultural Biotechnology Centre, Food Futures Institute, Murdoch University, Murdoch, WA, Australia.

Abstract

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.

Keywords: abiotic stress; antioxidant; drought; gene ontology; genomics; legume; miRNAs; stress responses.