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Duplication of AP1 within the Spinacia oleracea L. AP1/FUL clade is followed by rapid amino acid and regulatory evolution

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Abstract

The AP1/FUL clade of MADS box genes have undergone multiple duplication events among angiosperm species. While initially identified as having floral meristem identity and floral organ identity function in Arabidopsis, the role of AP1 homologs does not appear to be universally conserved even among eudicots. In comparison, the role of FRUITFULL has not been extensively explored in non-model species. We report on the isolation of three AP1/FUL genes from cultivated spinach, Spinacia oleracea L. Two genes, designated SpAPETALA1-1 (SpAP1-1) and SpAPETALA1-2 (SpAP1-2), cluster as paralogous genes within the Caryophyllales AP1 clade. They are highly differentiated in the 3′, carboxyl-end encoding region of the gene following the third amphipathic alpha-helix region, while still retaining some elements of a signature AP1 carboxyl motifs. In situ hybridization studies also demonstrate that the two paralogs have evolved different temporal and spatial expression patterns, and that neither gene is expressed in the developing sepal whorl, suggesting that the AP1 floral organ identity function is not conserved in spinach. The spinach FRUITFULL homolog, SpFRUITFULL (SpFUL), has retained the conserved motif and groups with Caryophyllales FRUITFULL homologs. SpFUL is expressed in leaf as well as in floral tissue, and shows strong expression late in flower development, particularly in the tapetal layer in males, and in the endothecium layer and stigma, in the females. The combined evidence of high rates of non-synonymous substitutions and differential expression patterns supports a scenario in which the AP1 homologs in the spinach AP1/FUL gene family have experienced rapid evolution following duplication.

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Abbreviations

AP1 :

APETALA1 gene

Fl :

FRUITFULL-LIKE gene

FUL :

FRUITFULL gene

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  1. D. Noah Sather

    Present address: Seattle Biomedical Research Institute, 307 Westlake Avenue N, Seattle, WA, 98109-5219, USA

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  1. Department of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA

    D. Noah Sather & Edward M. Golenberg

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Correspondence to Edward M. Golenberg.

Electronic supplementary material

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425_2008_851_MOESM1_ESM.pdf

Clustal –like alignment of translated amino acid sequences from FUL gene clade. The asterisks (*) indicate identical residues at a position, whereas the colon (:) indicates chemically similar residues at a position. The dashes (-) in the sequences indicate gaps inserted for alignment purposes (PDF 32 kb)

425_2008_851_MOESM2_ESM.pdf

Clustal –like alignment of translated amino acid sequences from AP1 gene clade. The asterisks (*) indicate identical residues at a position, whereas the colon (:) indicates chemically similar residues at a position. The dashes (-) in the sequences indicate gaps inserted for alignment purposes (PDF 33 kb)

425_2008_851_MOESM3_ESM.jpg

Unrooted phylogenetic gene trees of FUL and AP1 subtrees based on nucleotide and amino acid sequences of the variable C region alone. Data alignment was hypothesize within each subclades. a Neighbor-joining tree of the FUL subclade using the C region nucleotide sequences. b Mimimum-linkage tree of the FUL subclade using the translated C region nucleotide sequences. c Neighbor-joining tree of the AP1 subclade using the C region nucleotide sequences. d Neighbor-joining tree of the AP1 subclade using the translated C region nucleotide sequences

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Sather, D.N., Golenberg, E.M. Duplication of AP1 within the Spinacia oleracea L. AP1/FUL clade is followed by rapid amino acid and regulatory evolution. Planta 229, 507–521 (2009). https://doi.org/10.1007/s00425-008-0851-9

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