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ARABIDILLO gene homologues in basal land plants: species-specific gene duplication and likely functional redundancy

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Abstract

ARABIDILLO proteins regulate multicellular root development in Arabidopsis thaliana. Conserved ARABIDILLO homologues are present throughout land plants, even in early-evolving plants that do not possess complex root architecture, suggesting that ARABIDILLO genes have additional functions. Here, we have cloned and characterised ARABIDILLO gene homologues from two early-evolving land plants, the bryophyte Physcomitrella patens and the lycophyte Selaginella moellendorffii. We show that two of the PHYSCODILLO genes (PHYSCODILLO1A and -1B) exist as a tail-to-tail tandem array of two almost identical 12 kb sequences, while a third related gene (PHYSCODILLO2) is located elsewhere in the Physcomitrella genome. Physcomitrella possesses a very low percentage of tandemly arrayed genes compared with the later-evolving plants whose genomes have been sequenced to date. Thus, PHYSCODILLO1A and -1B genes represent a relatively unusual gene arrangement. PHYSCODILLO promoters are active largely in the haploid gametophyte, with additional activity at the foot of the sporophyte. The pattern of promoter activity is uniform in filamentous and leafy tissues, suggesting pleiotropic gene functions and likely functional redundancy: the latter possibility is confirmed by the lack of discernible phenotype in a physcodillo2 deletion mutant. Interestingly, the pattern of PHYSCODILLO promoter activity in female reproductive organs is strikingly similar to that of an Arabidopsis homologue, suggesting co-option of some PHYSCODILLO functions or regulation into both the sporophyte and gametophyte. In conclusion, our work identifies and characterises some of the earliest-evolving land plant ARABIDILLO homologues. We confirm that all land plant ARABIDILLO genes arose from a single common ancestor and suggest that PHYSCODILLO proteins have novel and pleiotropic functions, some of which may be conserved in later-evolving plants.

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Abbreviations

CHS:

Chalcone synthase

GUS:

β-Glucuronidase

HSP:

Heat shock promoter

MYA:

Million years ago

TAG:

Tandemly arrayed gene

UTR:

Untranslated region

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Acknowledgments

We thank Chris Franklin for useful discussions. We thank Drs. Yasuko Kamisugi and Andrew Cuming, University of Leeds, UK, for the kind gift of the pAHG1 vector. This work was funded by a Leverhulme Trust Research Project Grant (F/00094/BA) and a Royal Society Research Grant (RG081075) to JC, a Biotechnology and Biological Sciences Research Council Doctoral Training Grant to LAM and a Nuffield Foundation Undergraduate Research bursary to ES. Sequencing was carried out at the University of Birmingham Functional Genomics and Proteomics Unit.

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The authors declare that they have no conflict of interest.

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Correspondence to Juliet C. Coates.

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Moody, L.A., Saidi, Y., Smiles, E.J. et al. ARABIDILLO gene homologues in basal land plants: species-specific gene duplication and likely functional redundancy. Planta 236, 1927–1941 (2012). https://doi.org/10.1007/s00425-012-1742-7

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