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Molecular Evolution of FLORICAULA/LEAFY Orthologs in the Andropogoneae (Poaceae)

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Molecular Evolution of FLORICAULA/LEAFY Orthologs in the Andropogoneae (Poaceae) Molecular Evolution of FLORICAULA/LEAFY Orthologs in the Andropogoneae (Poaceae) Kirsten Bomblies1 and John F. Doebley Department of Genetics, University of Wisconsin-Madison Members of the grass family (Poaceae) exhibit a broad range of inflorescence structures and other morphologies, making the grasses an interesting model system for studying the evolution of development. Here we present an analysis of the molecular evolution of FLORICAULA/LEAFY-like genes, which are important developmental regulatory loci known to affect inflorescence development in a wide range of flowering plant species. We have focused on sequences from the Andropogoneae, a tribe within the grass family that includes maize (Zea mays ssp. mays) and Sorghum (Sorghum bicolor). The FLORICAULA/LEAFY gene phylogeny we generated largely agrees with previously published phylogenies for the Andropogoneae using other nuclear genes but is unique in that it includes both members of one of the many duplicate gene sets present in maize. The placement of these sequences in the phylogeny suggests that the duplication of the maize FLO- RICAULA/LEAFY orthologs, zfl1 and zfl2, is a consequence of a proposed tetraploidy event that occurred in the common Downloaded from https://academic.oup.com/mbe/article/22/4/1082/1083392 by guest on 01 October 2021 ancestor of Zea and a closely related genus, Tripsacum. Our data are consistent with the hypothesis that the transcribed regions of the FLORICAULA/LEAFY-like genes in the Andropogoneae are functionally constrained at both nonsynon- ymous and synonymous sites and show no evidence of directional selection. We also examined conservation of short noncoding sequences in the first intron, which may play a role in gene regulation. Finally, we investigated the genetic diversity of one of the two maize FLORICAULA/LEAFY orthologs, zfl2, in maize and its wild ancestor, teosinte (Z. mays ssp. parviglumis), and found no evidence for selection pressure resulting from maize domestication within the zfl2-coding region. Introduction Flower-bearing reproductive structures or inflorescen- in reproductive development. These include roles in shoot ces of angiosperms (flowering plants) vary dramatically in apical meristem development in tobacco (Ahearn et al. form and complexity. The grass family (Poaceae), which 2001), leaf compounding in pea and tomato (Souer et al. contains numerous closely related species with diverse 1998; Molinero-Rosales et al. 1999), and a potential role inflorescence phenotypes, is particularly striking in this in inflorescence branching in rice (Kyozuka et al. 1998). regard (Kellogg 2000), providing a useful model for the Furthermore, expression changes of FLO/LFY-like genes evolution of reproductive morphology in plants. To begin have been implicated in the evolution of inflorescence understanding the genetics underlying the evolution of architecture in Brassicaceae species (Shu et al. 2000; Yoon morphological structures, it is important to investigate the and Baum 2004), while in maize we have previously pro- molecular evolution of regulatory genes involved in the posed one of two duplicate FLO/LFY orthologs, zfl2, as a development of the phenotypes in question. candidate gene for a quantitative trait locus (QTL) contri- The genetic basis of the complex morphological buting to inflorescence structure differences between maize changes that accompany the transition to reproductive and its wild progenitor, teosinte (Zea mays ssp. parviglu- development has been extensively studied in flowering mis; hereafter parviglumis; Bomblies et al. 2003; Doebley plants,particularly indicot species.One ofthe keyregulatory 2004). The potential roles of FLO/LFY genes in inflores- genes in inflorescence and flower development is the cence structure evolution, along with the finding that these Antirrhinum majus FLORICAULA gene (FLO; Coen et al. genes appear to be involved in inflorescence branching in 1990) and its Arabidopsis thaliana ortholog, LEAFY the grasses rice and maize (Kyozuka et al. 1998; Bomblies (LFY; Weigel et al. 1992). FLO and LFY gene products et al. 2003), make them attractive candidates for a role in are involved in promoting the reproductive transition, as mediating the evolution of inflorescence structure differen- well as in controlling the identity and patterning of flowers ces in the Poaceae. and their constituent organs (Coen et al. 1990; Weigel et al. To begin addressing whether FLO/LFY orthologs 1992). Studies in additional species suggest that the role of may play a role in grass morphological evolution, we FLO/LFY orthologs in reproductive development is largely undertook a study of the molecular evolution of FLO/ conserved in diverse angiosperms, including maize (Hofer LFY-like genes in the Andropogoneae, a morphologically et al. 1997; Souer et al. 1998; Molinero-Rosales et al. diverse tribe of grasses that includes maize and sorghum 1999; Ahearn et al. 2001; Bomblies et al. 2003). (Kellogg 2000). We generated a phylogeny for Andropo- In some species the FLO/LFY genes appear to have goneae FLO/LFY-like genes and studied their molecular evolved novel functions in addition to their normal roles evolution. We also examined nucleotide diversity at the zfl2 locus in maize and parviglumis to address whether this 1 Present address: Department of Molecular Biology, Max Planck gene has been selected for inflorescence architecture differ- Institute for Developmental Biology, Spemannstrasse 37-39, Tu¨bingen, ences during the domestication of maize. Taken together, Germany. our results suggest that the FLO/LFY-like genes in the Key words: FLORICAULA/LEAFY, Andropogoneae, zfl1, zfl2, maize, domestication. Andropogoneae are evolving with selective constraint for amino acid conservation. Relative-rate tests on zfl1- and E-mail: [email protected]. zfl2-like sequences in maize and its close relatives suggest Mol. Biol. Evol. 22(4):1082–1094. 2005 doi:10.1093/molbev/msi095 that in most species neither of the paralogs shows strong Advance Access publication February 2, 2005 evidence for relaxed constraint following duplication. Molecular Biology and Evolution vol. 22 no. 4 Ó Society for Molecular Biology and Evolution 2005; all rights reserved. Molecular Evolution of Andropogoneae FLO/LFY Genes 1083 Table 1 Species Used for Sequencing of FLO/LFY Orthologs Sample Paraloga Origin Source Collection GenBank Accession Number Panicoideae, Andropogoneae Apluda mutica India USDA PI 271556 AY789607 Bothriochloa odorata India USDA PI 301632 AY789616 Capillipedium parviflorum India USDA PI 301782 AY789618 Chionachne koenigii RES 97-18 AY789614 Chrysopogon fulvus Pakistan USDA PI 199241 AY789611 Cleistachne sorghoides ICRISAT IS 14346 AY789619 Coelorachis aurita Paraguay USDA PI 404628 AY789606 Coelorachis selloana Brazil USDA PI 309987 AY789608 Coix aquatica JFW 2-88 AY789609 Coix lacyrma-jobi Brazil USDA PI 320865 AY789624 Cymbopogon distans India USDA PI 271552 AY789610 Downloaded from https://academic.oup.com/mbe/article/22/4/1082/1083392 by guest on 01 October 2021 Cymbopogon flexuosus USDA PI 209700 AY789617 Elionurus muticus EAK JS 5865 AY789605 Elionurus tripsacoides Texas JD 646 AY789604 Heteropogon contortus South Africa USDA PI 364892 AY789612 Hyparrhenia hirta Ethiopia USDA PI 196827 AY789615 Ischaemum afrum South Africa USDA PI 364923 AY789620 Phacelurus digitatus Turkey USDA PI 206746 AY789613 Saccharum officinarum LL UMGH AY789622 Sorghum bicolor ICRISAT IS 12711 AY789623 Sorghum versicolor Ethiopia USDA PI 260273 AY789621 Tripsacum andersonii zfl1 DT 68-68 AY789595 zfl2 AY789600 zfl2(m) AY789599 Tripsacum dactyloides zfl1 United States DT 68-23-5 AY789596 Tripsacum floridanum zfl1 United States 68-23-5 AY789590 zfl2 AY789601 Tripsacum latifolium zfl1 DT 79-20 AY789592 Tripsacum zopilotense zfl1 Mexico 79-74 AY789591 zfl2 AY789602 Zea diploperennis zfl2 RG 1120 AY789598 Zea luxurians zfl1 HI G-5 AY789594 zfl2 AY780597 Zea mays zfl1 United States JK W22 AY789593 zfl2 AY789603 Panicoideae, Arundinelleae Arundinella hirta Japan USDA PI 246756 AY789625 NOTE.—DT 5 David Timothy; EAK 5 Elizabeth A. Kellogg; HI 5 Hugh Iltis; JD 5 John Doebley; JFW 5 Jonathan F. Wendel; JK 5 Jerry Kermicle; ICRISAT 5 International Crops Research Institute for Semi-Arid Tropics; LL 5 Lewis Lukens; RES 5 Russell E. Spangler; RG 5 Rafael Guzman; UMGH 5 University of Minnesota Greenhouse; USDA 5 United States Department of Agriculture. a Paralog 5 sequence similarity to maize zfl1 or zfl2 for tetraploid clade (Zea and Tripsacum); zfl2(m) 5 maize-like zfl2 allele from T. andersonii. Finally, though we have previously presented zfl2 as a can- M13R, and internal primers. Inserts were sequenced to at didate gene for a maize domestication QTL based on its least 23 coverage from multiple clones to correct for Taq roles in development, there is no significant evidence for error. We manually edited sequences using Sequencher a selective sweep having acted on the zfl2-transcribed 4.1 (GeneCodes Corporation, Ann Arbor, Mich.) generated region during domestication. alignments using ClustalW (Thompson, Higgins, and Gibson 1994), and manually edited alignments in Se-Al v.1.0a1 (Rambaut 1996). Andropogoneae sequences are Materials and Methods available in GenBank (accession numbers AY789590– Sample Material and Sequencing AY789625; see Supplementary Material). We amplified FLO/LFY-like gene sequences by poly- We sampled zfl2 diversity in maize from a geograph- merase chain reaction (PCR) from 29 Andropogoneae spe- ically diverse collection of 16 maize landraces as previously cies in 18 genera and one out-group (Arundinella
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