Evolutionary history and functional diversification of WOX genes in Annona Atemoya

TL;DR

This study explores the WOX gene family in Annona atemoya, revealing their roles in plant development and regeneration through evolutionary and functional analysis.

Contribution

The study provides the first genome-wide analysis of WOX genes in Annona atemoya, uncovering their evolutionary conservation and functional divergence.

Findings

Eleven WOX genes were identified and classified into three clades with conserved structures and regulatory motifs.

AaWOX1 and AaWOX3 are highly expressed in shoot tissues and during shoot regeneration.

AaWUS is strongly induced during callus formation, suggesting a role in cellular reprogramming.

Abstract

WUSCHEL-related homeobox (WOX) transcription factors play pivotal roles in plant development and evolutionary innovation. However, their functions remain largely unexplored in the basal angiosperm Annona atemoya, an economically significant species. This study aimed to elucidate the role of the WOX gene family in growth and regeneration in atemoya using genome-wide identification and functional characterization.

In the atemoya genome, 11 WOX genes were identified and phylogenetically classified into three distinct clades: Ancient, Intermediate, and Modern. This classification was confirmed by their conserved gene structures and motif compositions. A comparative genomic analysis revealed conserved synteny and purifying selection (Ka/Ks < 1) among WOX orthologs of atemoya, Amborella, and Arabidopsis, highlighting evolutionary constraints and essential functional roles. Analysis of promoters in cis-elements showed the enrichment of development- and hormone-responsive motifs, indicating that AaWOX genes are integrated in conserved regulatory networks. Tissue-specific expression profiling revealed divergent spatiotemporal patterns. AaWOX1 and AaWOX3 were highly expressed in shoot tissues and during shoot regeneration. AaWOX11/12 and AaWOX5/7 were preferentially expressed in roots, but only AaWOX11/12 was significantly upregulated during root regeneration. Notably, AaWUS was almost undetectable in normal roots but became strongly induced upon callus formation, implying a role in de-differentiation and cellular reprogramming.

Our study provides a comprehensive genome-wide analysis of the AaWOX family in atemoya, revealing its clade-specific evolutionary conservation and putative functional divergence during organ development and regeneration. These findings highlight the pivotal roles of WOX transcription factors in coordinating regenerative responses in a basal angiosperm and establish a critical foundation for the genetic improvement and biotechnology applications in Annona atemoya.

The online version contains supplementary material available at 10.1186/s12870-026-08109-5.

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