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Wound-inducible WUSCHEL-RELATED HOMEOBOX 13 is required for callus growth and organ reconnection.

ABSTRACT: Highly efficient tissue repair is pivotal for surviving damage-associated stress. Plants generate callus upon injury to heal wound sites, yet regulatory mechanisms of tissue repair remain elusive. Here, we identified WUSCHEL-RELATED HOMEOBOX 13 (WOX13) as a key regulator of callus formation and organ adhesion in Arabidopsis (Arabidopsis thaliana). WOX13 belongs to an ancient subclade of the WOX family, and a previous study shows that WOX13 orthologs in the moss Physcomitrium patens (PpWOX13L) are involved in cellular reprogramming at wound sites. We found that the Arabidopsis wox13 mutant is totally defective in establishing organ reconnection upon grafting, suggesting that WOX13 is crucial for tissue repair in seed plants. WOX13 expression rapidly induced upon wounding, which was partly dependent on the activity of an AP2/ERF transcription factor, WOUND-INDUCED DEDIFFERENTIATION 1 (WIND1). WOX13 in turn directly upregulated WIND2 and WIND3 to further promote cellular reprogramming and organ regeneration. We also found that WOX13 orchestrates the transcriptional induction of cell wall-modifying enzyme genes, such as GLYCOSYL HYDROLASE 9Bs, PECTATE LYASE LIKEs and EXPANSINs. Furthermore, the chemical composition of cell wall monosaccharides was markedly different in the wox13 mutant. These data together suggest that WOX13 modifies cell wall properties, which may facilitate efficient callus formation and organ reconnection. Furthermore, we found that PpWOX13L complements the Arabidopsis wox13 mutant, suggesting that the molecular function of WOX13 is partly conserved between mosses and seed plants. This study provides key insights into the conservation and functional diversification of the WOX gene family during land plant evolution.

SUBMITTER: Ikeuchi M

PROVIDER: S-EPMC8774835 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Bamboos (Bambusoideae) are fast-growing species due to their rapid growth rate and ability to reproduce annually via cloned buds produced on the rhizome. WUSCHEL-related homeobox (WOX) genes have been reported to regulate shoot apical meristem organization, lateral organ formation, cambium and vascular proliferation, and so on, but have rarely been studied in bamboos. In this study, the WOXs of both herbaceous bamboo species (12 OlaWOXs and nine RguWOXs) and woody bamboo species (18 GanWOXs, 27 PheWOXs, and 26 BamWOXs) were identified and categorized into three clades based on their phylogenetic relationship-ancient, intermediate, or WUS clade. Polyploidy is the major driver of the expansion of the bamboo WOX family. Eight conserved domains, besides the homeodomain, were identified by comparatively analyzing the WOXs of dicot and monocot species. Intensive purifying selection pressure in the coding region of specific domains explained the functional similarity of WOXs between different species. For Bambusoideae WOXs, polyploidy is the major driver of the expansion of the WOX family. Stronger purifying selection was found in orthologous WOXs of Bambusoideae, especially for WOX4s and WOX5s, which are conserved not only at the translational levels, but also at the genome level. Several conserved cis-acting elements were discovered at similar position in the promoters of the orthologous WOXs. For example, AP2/ERF protein-binding elements and B3 protein-binding elements were found in the promoters of the bamboo WOX4, while MYB protein-binding elements and Dof protein-binding elements were found in the promoters of bamboo WOX5, and MADS protein-binding sites was found in the promoters of bamboo WUS, WOX3, and WOX9. These conserved positions may play an important role in regulating the expression of bamboo WOXs. Our work provides insight into the origin and evolution of bamboo WOXs, and will facilitate functional investigations of the clonal propagation of bamboos.

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Wound-inducible WUSCHEL-RELATED HOMEOBOX 13 is required for callus growth and organ reconnection.

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