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Duplication of the Asymmetric Leaves1/Rough Sheath 2/Phantastica (ARP) gene precedes the explosive radiation of the Ruschioideae

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Abstract

The Mesembryanthemoideae and Ruschioideae subfamilies are a major component of the Greater Cape Floristic Region in southern Africa. The Ruschioideae show an astonishing diversity of leaf shape and growth forms. Although 1,585 species are recognised within the morphologically diverse Ruschioideae, these species show minimal variation in plastid DNA sequence. We have investigated whether changes in selected leaf development transcription factors underpin the recent, rapid diversification of this large group of succulent plants. Degenerate primers designed to conserved regions of Asymmetric Leaves1/Rough Sheath 2/Phantastica (ARP) and the Class III HD-ZIP family of genes, were used to amplify sequences corresponding to these genes from several species within the Mesembryanthemoideae and Ruschioideae subfamilies. Two members of the Class III HD-ZIP family were identified in both the Mesembryanthemoideae and Ruschioideae, and were derived from an ancient gene duplication event that preceded the divergence of gymnosperms and angiosperms. While a single ARP orthologue was identified in the Mesembryanthemoideae, two paralogues, ARPa and ARPb, were identified in the Ruschioideae subfamily. ARPa was present in all species of Ruschioideae analysed in this study. ARPb has been lost from the Apatesieae and Dorotheantheae tribes, which form an early evolutionary branch from the Ruschieae tribe, as well as from selected species within the Ruschieae. The recent duplication and subsequent selected gene loss of the ARP transcription factor correlates with the rapid diversification of plant forms in the Ruschioideae.

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Acknowledgements

This research was supported with funding from the University of Cape Town Research Committee. We thank the following MCB3012Z third year project students who also contributed data in this manuscript: Hermien Fourie, Abigail Hlambelo, Britta Kleeman, Janet Lyons-Lewis, Romaney Pinnock, Anita Buramu, Joern Laemke. Peter Linder is thanked for constructive criticism of the manuscript.

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Authors and Affiliations

  1. Department of Molecular and Cell Biology, University of Cape Town, Private Bag, Rondebosch, 7701, Cape Town, South Africa

    Nicola Illing, Cheryl Johnson, Denise Brito, Nuria Negrao, Fiona Baine, Victoria van Kets, Kayshinee Rye Ramchurn & Laura Roden

  2. Department of Botany, University of Cape Town, Private Bag, Rondebosch, 7701, Cape Town, South Africa

    Cornelia Klak

  3. Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Private Bag, Rondebosch, 7701, Cape Town, South Africa

    Cathal Seoighe

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  1. Nicola Illing
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  2. Cornelia Klak
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  3. Cheryl Johnson
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  4. Denise Brito
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  5. Nuria Negrao
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  6. Fiona Baine
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  7. Victoria van Kets
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  8. Kayshinee Rye Ramchurn
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  9. Cathal Seoighe
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  10. Laura Roden
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Corresponding author

Correspondence to Nicola Illing.

Additional information

Communicated by K. Schneitz

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Table S1

List of Genbank Accession Numbers used in this study. (DOC 77 kb)

Fig. S1

Phylogram of the ARP gene family in the selected angiosperms, Mesembryanthemoideae and Ruschioideae constructed with PhyML, based on a ClustalW alignment of coding regions amplified by AS1_F and AS1_R degenerate primers. The duplication of ARP in legumes is highlighted in lime green, and is indicated by a green arrow. A. majus and A. thaliana which have a single copy of ARP are highlighted in sea green. Species within the Mesembryanthemoideae are indicated in black. Duplication of ARP into ARPa and ARPb after diversification of the Ruschioideae from the Mesembryanthemoideae is indicated with a black arrow. Species within the Dorotheantheae and Apatesieae tribes are indicated in purple, whilst ARPa and ARPb in the Ruschieae are indicated in blue and magenta, respectively. Pseudogenes were excluded from this analysis. Percentage values from the approximate likelihood ratio test are indicated at nodes. 190 × 275 mm (96 × 96 DPI)

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Illing, N., Klak, C., Johnson, C. et al. Duplication of the Asymmetric Leaves1/Rough Sheath 2/Phantastica (ARP) gene precedes the explosive radiation of the Ruschioideae. Dev Genes Evol 219, 331–338 (2009). https://doi.org/10.1007/s00427-009-0293-9

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