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Unraveling the evolution and regulation of the alternative oxidase gene family in plants

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Abstract

Alternative oxidase (AOX) is a diiron carboxylate protein present in all plants examined to date that couples the oxidation of ubiquinol with the reduction of oxygen to water. The predominant structure of AOX genes is four exons interrupted by three introns. In this study, by analyzing the genomic sequences of genes from different plant species, we deduced that intron/exon loss/gain and deletion of fragments are the major mechanisms responsible for the generation and evolution of AOX paralogous genes. Integrating gene duplication and structural information with expression profiles for various AOXs revealed that tandem duplication/block duplication contributed greatly to the generation and maintenance of the AOX gene family. Notably, the expression profiles based on public microarray database showed highly diverse expression patterns among AOX members in different developmental stages and tissues and that both orthologous and paralogous genes did not have the same expression profiles due to their divergence in regulatory regions. Comparative analysis of genes in six plant species under various perturbations indicated a large number of protein kinases, transcription factors and antioxidant enzymes are co-expressed with AOX. Of these, four sets of transcription factors—WRKY, NAC, bZIP and MYB—are likely involved in the regulating the differential responses of AOX1 genes to specific stresses. Furthermore, divergence of AOX1 and AOX2 subfamilies in regulation might be the main reason for their differential stress responses.

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Acknowledgments

We would like to thank Prof. J.C.M. (Sjef) Smeekens and Dr. Alessia Peviani at Utrecht University, for their helpful advice in visualizing phylogenetic tree, and our lab members, Ting-Hong Tan for providing plant picture. This study was supported by the National Natural Science Foundation of China (31470342, 91417305, 31400211), the National Basic Research Program of China (973 Program) (2015CB150100), and Sichuan Natural Science Foundation (2015JY0101, 2015JY0223).

We thank anonymous reviewers for helpful comments on the paper.

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Authors and Affiliations

  1. Ministry of Education Key Laboratory for Bio-Resource and Eco-Environment, State Key Laboratory of Hydraulics and Mountain River Engineering, College of Life Science, Sichuan University, Chengdu, 610064, China

    Xiao-jun Pu, Xin Lv & Hong-hui Lin

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  1. Xiao-jun Pu
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  2. Xin Lv
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  3. Hong-hui Lin
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Correspondence to Hong-hui Lin.

Additional information

Communicated by Sureshkumar Balasubramanian

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Fig. S1aFig. S1b

Three-dimensional structure of predicted AOX. Amino acid residues involved in the diiron active site are shown as pink spheres and hydrogen bonds are indicated by white color. Accession numbers for each gene are listed in supplementary table S1. Three-dimensional structure of AOX Proteins were predicted by the I-TASSER server. The figures were prepared with Pymol1.6 (http://www.pymol.org/). (GIF 3063 kb)

The dimerization potential of AOX. (GIF 5774 kb)

High resolution image (TIFF 22666 kb)

High resolution image (TIFF 35441 kb)

Fig. S2

Gene expression profiles of AOX gene family across a diversity of plant species over the development stage. Error bars represent standard error. Data were retrieved from the Genevestigator microarray database (https://www.genevestigator.com/gv/plant.jsp) using development tools. (GIF 3252 kb)

High resolution image (TIFF 5789 kb)

Fig. S3

a-h Expression profiles of the AOX gene family from some plants. The figure represents the average of expression value of log2-scale from diverse tissues or organs of plants and displayed as nodes of a tree which children nodes are included into parent nodes that reflect number of the samples. Error bars indicated standard error. Data were obtained from the Genevestigator microarray database using anatomy tools. (GIF 826 kb)

High resolution image (TIFF 5157 kb)

(PNG 561 kb)

Fig. S4

A-D Heat map of co-expressed genes. The co-expression analysis was conducted by using Genevestigator co-expression tools with the parameters of 2 log2 fold change and p ≤ 0.05 was used as cut-off. The maximum number of genes for each co-expressed gene lists is 100. (Zimmermann et al., 2008; Hruz et al., 2008). For GO annotations, the co-expressed gene lists generated from co-expression tools were loaded into agriGO (Du et al., 2010) for further analysis with suggested parameters. Hierarchical clustering was conducted by Genevestigator-hierarchical clustering tools using Euclidean distance (Prelic et al., 2006). (GIF 4526 kb)

(GIF 1771 kb)

(GIF 2145 kb)

(GIF 24884 kb)

High resolution image (TIFF 56024 kb)

High resolution image (TIFF 10779 kb)

High resolution image (TIFF 5056 kb)

High resolution image (TIFF 15148 kb)

Fig. S5a-b

Multiple alignment of AOX and PTOX (GIF 4307 kb)

(GIF 4361 kb)

High resolution image (TIFF 14028 kb)

High resolution image (TIFF 14515 kb)

Fig. S6

GO annotations. (DOC 1086 kb)

Table S1

Original sequence identifiers for plant’s AOX gene. (XLS 40 kb)

Table S2

Putative cis-acting elements of AOX gene family member (DOC 119 kb)

Table S3a

Co-expression profiles of AOX-positive-correlation. (XLS 431 kb)

Table S3b

Co-expression profiles of AOX-negative-correlation. (XLS 531 kb)

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Pu, Xj., Lv, X. & Lin, Hh. Unraveling the evolution and regulation of the alternative oxidase gene family in plants. Dev Genes Evol 225, 331–339 (2015). https://doi.org/10.1007/s00427-015-0515-2

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