Duplication and diversification of the LEAFY HULL STERILE1 and Oryza sativa MADS5 SEPALLATA lineages in graminoid Poales

Ashley R Christensen,Simon T Malcomber

doi:10.1186/2041-9139-3-4

Ashley R Christensen, Simon T Malcomber

Open Access

https://doi.org/10.1186/2041-9139-3-4

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Abstract

BackgroundGene duplication and the subsequent divergence in function of the resulting paralogs via subfunctionalization and/or neofunctionalization is hypothesized to have played a major role in the evolution of plant form. The LEAFY HULL STERILE1 (LHS1) SEPALLATA (SEP) genes have been linked with the origin and diversification of the grass spikelet, but it is uncertain 1) when the duplication event that produced the LHS1 clade and its paralogous lineage Oryza sativa MADS5 (OSM5) occurred, and 2) how changes in gene structure and/or expression might have contributed to subfunctionalization and/or neofunctionalization in the two lineages.MethodsPhylogenetic relationships among 84 SEP genes were estimated using Bayesian methods. RNA expression patterns were inferred using in situ hybridization. The patterns of protein sequence and RNA expression evolution were reconstructed using maximum parsimony (MP) and maximum likelihood (ML) methods, respectively.ResultsPhylogenetic analyses mapped the LHS1/OSM5 duplication event to the base of the grass family. MP character reconstructions estimated a change from cytosine to thymine in the first codon position of the first amino acid after the Zea mays MADS3 (ZMM3) domain converted a glutamine to a stop codon in the OSM5 ancestor following the LHS1/OSM5 duplication event. RNA expression analyses of OSM5 co-orthologs in Avena sativa, Chasmanthium latifolium, Hordeum vulgare, Pennisetum glaucum, and Sorghum bicolor followed by ML reconstructions of these data and previously published analyses estimated a complex pattern of gain and loss of LHS1 and OSM5 expression in different floral organs and different flowers within the spikelet or inflorescence.ConclusionsPrevious authors have reported that rice OSM5 and LHS1 proteins have different interaction partners indicating that the truncation of OSM5 following the LHS1/OSM5 duplication event has resulted in both partitioned and potentially novel gene functions. The complex pattern of OSM5 and LHS1 expression evolution is not consistent with a simple subfunctionalization model following the gene duplication event, but there is evidence of recent partitioning of OSM5 and LHS1 expression within different floral organs of A. sativa, C. latifolium, P. glaucum and S. bicolor, and between the upper and lower florets of the two-flowered maize spikelet.

Highlights

Gene duplication and the subsequent divergence in function of the resulting paralogs via subfunctionalization and/or neofunctionalization is hypothesized to have played a major role in the evolution of plant form
To further investigate support for the estimated relationships we employed a Shimodaira-Hasegawa (SH) test [32] to compare the best maximum likelihood (ML) tree from the Bayesian search with the best ML tree satisfying the constraint that the LEAFY HULL STERILE1 (LHS1)/Oryza sativa MADS5 (OSM5) duplication occurred at the base of the BEP+PACCMAD clades
This analysis estimated the constraint tree (-ln 29886.59) as significantly less likely than the unconstrained analysis (-ln 23530.75, P < 0.001). These data suggest that the LHS1/OSM5 (L1O5) duplication event occurred at the base of the grass family

Summary

Introduction

Gene duplication and the subsequent divergence in function of the resulting paralogs via subfunctionalization and/or neofunctionalization is hypothesized to have played a major role in the evolution of plant form. The diversification of paralogs following developmental gene duplication events is hypothesized to have played a major role in the evolution of morphological form [1,2,3]. At the base of each grass spikelet are two bractlike structures called glumes and each grass floret typically contains a lemma, a palea, two lodicules, three stamens, and a pistil. Joinvilleaceae and Ecdeiocoleaceae, in addition to other non-grass members of the graminoid Poales clade, have typical monocot flowers suggesting that a series of profound developmental and genetic changes occurred early in the history of the Poaceae lineage to produce grass spikelets, glumes, lemmas, paleas and lodicules typical of most taxa within the family

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