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First published online September 11, 2009; 10.1105/tpc.109.068239 The Plant Cell 21:2591-2605 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Evolution of AGL6-like MADS Box Genes in Grasses (Poaceae): Ovule Expression Is Ancient and Palea Expression Is New[W],[OA]Department of Biology, University of Missouri, St. Louis, Missouri 63121 1 Address correspondence to reinheimerr{at}umsl.edu.
AGAMOUS-like6 (AGL6) genes encode MIKC-type MADS box transcription factors and are closely related to SEPALLATA and AP1/FUL-like genes. Here, we focus on the molecular evolution and expression of the AGL6-like genes in grasses. We have found that AGL6-like genes are expressed in ovules, lodicules (second whorl floral organs), paleas (putative first whorl floral organs), and floral meristems. Each of these expression domains was acquired at a different time in evolution, indicating that each represents a distinct function of the gene product and that the AGL6-like genes are pleiotropic. Expression in the inner integument of the ovule appears to be an ancient expression pattern corresponding to the expression of the gene in the megasporangium and integument in gymnosperms. Expression in floral meristems appears to have been acquired in the angiosperms and expression in second whorl organs in monocots. Early in grass evolution, AGL6-like orthologs acquired a new expression domain in the palea. Stamen expression is variable. Most grasses have a single AGL6-like gene (orthologous to the rice [Oryza sativa] gene MADS6). However, rice and other species of Oryza have a second copy (orthologous to rice MADS17) that appears to be the result of an ancient duplication.
The identity of floral organs in most angiosperms is specified by a combination of transcription factors in the MADS box family (Ng and Yanofsky, 2001  ). These transcription factors fall into large clades, often named for the characteristic protein in Arabidopsis thaliana, such as AGAMOUS, PISTILLATA, APETALA3, APETALA1, and SEPALLATA (Becker and Theissen, 2003). Whereas many of these clades of proteins have been studied extensively, others are much more poorly known. One of these less well-studied clades includes proteins that are coorthologous to the Arabidopsis protein AGL6.
Phylogenetic analysis of MADS box genes and/or proteins has shown that AGL6-like genes are sister to the SEPALLATA-like genes (E-function) (Purugganan et al., 1995
AGL6-like genes have been characterized as floral specific in several Angiosperms; however, some studies reported expression in vegetative tissues (Ma et al., 1991
Grasses are morphologically unique in having highly modified flowers (florets) collected into novel structures called spikelets (Clifford, 1987
AGL6-like genes in grasses might be involved in lodicule, stamen, carpel, and seed development. For instance, rice (Oryza sativa) has two AGL6-like genes, MADS6 and MADS17. Based on RNA gel blots, Moon et al. (1999)
The function of AGL6 genes during flower development in grasses as well in other lineages is therefore not clear, although they may play a role in perianth and gynoecium development. Given the characterization of a loss-of-function mutant for AGL6 in maize (Thompson et al., 2009
The AGL6-like Duplicate Genes Evolve at Different Rates To reconstruct the evolutionary history of AGL6-like genes in grasses, we PCR amplified AGL6-like genes from disparate grass species to supplement data available in GenBank (see Supplemental Table 3 online). Sequences spanned the three regions of the gene, the I (intervening, important for specification of dimerization), K (keratin-like, facilitates dimerization), and C (C terminus, functions as a transactivation region and contributes to the formation of multimeric MADS box protein complexes), regions but excluded the highly conserved MADS box and sometimes 25 bp at the 3' end of the C terminus. Most of the divergence among the sequences appears in the C-terminal region. All sequences had a single open reading frame and no premature stop codons. All amino acid sequences shared a conserved motif at the end of the C terminus (MLGWVL). The Oryza species investigated had two copies of AGL6-like genes, corresponding to MADS6 and MADS17, as previously described. We used two methods to assess the timing of the MADS6/MADS17 duplication and arrived at contradictory results. First, we determined the presence/absence of the two paralogs in grasses outside the genus Oryza. No homolog of MADS17 was found in the maize, sorghum (Sorghum bicolor), or Brachypodium genomes or in any other genome database (see Methods). In addition, multiple efforts at PCR and sequencing of multiple clones failed to detect MADS17-like sequences in other grasses or nongrass monocots; therefore, we conclude that MADS17 is truly absent in all grasses except Oryza. Within Oryza, the MADS17-like sequences (254 amino acids long) differ by 71 amino acids from the paralogous MADS6-like sequences (250 amino acids long) (see Supplemental Figure 1 online), with most substitutions located at the C terminus. Among the Oryza MADS17-like sequences, however, both coding regions and intron sequences were conserved. Taken together, these data suggest that MADS17 is the product of a duplication event at the origin of the genus Oryza. The second method we used to assess the timing of the MADS6/MADS17 duplication was to analyze the sequences phylogenetically; for this analysis, we retrieved similar trees for all analytical methods. Phylogenetic analysis offers a different estimate of the timing of the MADS6 and MADS17 duplication, which appears after the divergence of Restionaceae and before the divergence of Joinvilleaceae. However, we cannot reject the possibility that the duplication occurred at the same time as the whole-genome duplication of the grasses, after the divergence of Joinvilleaceae but before the origin of the family (Figure 1 ). The S-H test rejects all other possible placements of this duplication at P values < 0.05; statistical phylogenetic evidence thus argues against the possibility that the duplication was specific only to Oryza.
The branch leading to the Os MADS17 clade is the longest branch in the tree (Figure 1), and relative rates tests show that MADS17 has evolved significantly faster than MADS6 (P = 0.01963). Twenty-five amino acid substitutions characterized the MADS17 clade, and 17 are unique substitutions that do not change elsewhere in the clade (Figure 1, number in white box). Most of these mutations are located at the K-domain and C terminus. Nine substitutions change the chemical properties of the residues (i.e., 83 D-G, 94 T-H, 139 C-Y, 205 A-R, and 260 V-P) with the remainder being conservative substitutions (see Supplemental Figure 1 online). MADS17 orthologs also differ in the highly conserved motif that characterizes the MADS6-like sequences in the grasses (256-261 MLGWVL versus VMGWPL). In addition, MADS17 has an extra five amino acids at the N terminus of the MADS box (MDRSE) that are not found in other known AGL6-like genes or MADS box genes. The duplication of zag3 and zag5 (both genes of maize) may have occurred before the common ancestor of Zea plus Tripsacum. However, the duplication could have been before the common ancestor of Zea, Tripsacum, Sorghum, and Coix (the zag3/Td AGL6.2 + Sb AGL6 + Cos AGL6 clade). Neither relationship is well supported and cannot be distinguished statistically. There is no evidence that zag5/zag3 are evolving at different rates.
Within the Os MADS6 clade, the phylogeny largely agrees with that proposed for the grass family by the Grass Phylogeny Working Group (2001)
All AGL6-like genes are under purifying selection, although sites do not evolve homogeneously across the gene (see Supplemental Statistical Tests online; codons showed
AGL6 mRNA Expression Patterns
To determine tissue-specific patterns of AGL6 mRNA expression, we conducted in situ hybridizations on inflorescences of several grass species. The specificity of the probe was verified by DNA gel blot hybridization; in all cases, the probe detected a single band. In all species examined, AGL6 mRNA is first detected in floral meristems during early inflorescence development (Figures 3A and 3B ; O. sativa and Setaria italica are representative). No expression was detected in the main axis of the inflorescence and branches nor was there expression in glumes.
Joinvillea ascendens (Joinvilleaceae) has a typical monocot floral plan with three outer tepals, three inner tepals, six stamens and three carpels. Ja AGL6 was first detected in the inner tepal primordia as well as in the young anthers and gynoecium (carpels and ovule) (Figures 4A to 4C ). Later, expression in the inner tepals and carpels decreased, but expression was detectable in the stamens; gynoecial expression was restricted to the ovule (Figure 4D). Very early developmental stages were unavailable, so we could not check floral meristem expression.
In Streptochaeta angustifolia (Anomochlooideae), the spikelet equivalent has been described as a complex of 11 or 12 bracts (I to XII) that initiate before the stamens and carpels. Previous studies suggested that bracts VII to VIII (or IX) represent the outer whorl and bracts X to XII are modifications of the inner tepals or second whorl of a typical monocot flower (Whipple et al., 2007 ). Bracts X to XII initiate as a whorl outside the stamens and inside the VII-VIII-(IX) whorl. Sa AGL6 was first detected in the floral meristem (see Supplemental Figure 4 online) and subsequently in bracts X to XII as well as in young anthers and gynoecium (Figures 4E and 4F). Later, expression in bracts X to XII and in the carpels is reduced, but Sa AGL6 is still expressed in the anthers; gynoecial expression is restricted to the ovule (Figures 4G to 4I). We found no expression in bracts VII and VIII. Lithachne humilis (Bambusoideae) bears female and male spikelets in separate inflorescences. We observed the female inflorescences, which contain one spikelet with a female floret plus a basal sterile spikelet characterized by a single scale or a tiny vestige of a male spikelet. Lh AGL6 expression was detected in the female spikelet, but no expression was observed in the vestigial male basal spikelet (Figure 5A ). In the fertile spikelet, Lh AGL6 was detected in palea as well as in the carpel primordia (Figure 5B). Expression was not detected in what we assume are reduced lodicules. Very early developmental stages were unavailable, so we could not check floral meristem expression.
The O. sativa (Ehrhartoideae) spikelet contains three florets, one bisexual and fertile and two reduced to sterile lemmas. The glumes are tiny flaps of tissue below the sterile lemmas and are often known as rudimentary glumes. Os MADS6 mRNA was detected in young palea and stamen primordia (Figure 5C). Later in development, Os MADS6 mRNA was also detected in lodicules, gynoecium, and anther walls (Figures 5D and 5E). Still later, expression was only observed in the inner integument of the ovule (Figure 5F). The expression pattern of Os MADS17 is distinct from that of Os MADS6 starting at an early stage of development. Os MADS17 mRNA is initially detected in the floral meristem (Figure 3A) and later becomes restricted to a group of cells next to the developing lemma that we interpret as young lodicule primordia. No expression was detected in the young palea primordium or in any other region of the floral meristem (Figure 5G). Later, expression was also observed in lodicules and in the anther wall, but no significant expression was detected in the carpels and inner integument (Figures 5H and 5I). Lolium temulentum and Triticum monococcum (Pooideae) have inflorescences comprised of sessile spikelets with each spikelet containing four to 10 and two to eight florets, respectively, subtended by one (Lolium) or two glumes (Triticum). Lt AGL6 and Tm AGL6 show the same pattern of expression within spikelets. Both genes are expressed in palea, lodicules, and carpels (Figures 6A to 6C ; only in situs of T. monoccocum are shown). In addition, AGL6-like genes are expressed in floral meristems in both species (see Supplemental Figure 4 online).
Eleusine indica (Chloridoideae) has sessile spikelets containing three to 15 florets subtended by two glumes. Within a spikelet, Ei AGL6 mRNA is detected in the distal floral meristems as well as in floral organs of the proximal florets, which are more advanced in development (Figure 6D). Ei AGL6 is expressed in the palea, lodicules, and carpel primordia (Figures 6E). Later, Ei AGL6 mRNA was only detected in the inner integument of the ovule (Figure 6F). S. bicolor (Panicoideae) has an inflorescence comprised of pedicellate and sessile spikelets, each of which includes two florets. Florets in the spikelet mature basipetally. The upper floret of the sessile spikelet is bisexual, whereas the upper floret of the pedicellate spikelet is staminate or sterile, with the pistil aborting early in development. In upper florets, the lemma and palea wrap around the flower with the margins of the palea inserted inside the margins of the lemma; this means that sections will often capture the palea and lemma on both sides of the floral organs. The lower floret in both the sessile and pedicellate spikelets includes only a floral meristem and a sterile lemma. Sb AGL6 is expressed throughout the floral meristem (delimited by the corresponding lemma) of both florets in the sessile and pedicellate spikelet (Figure 7A ) and later is detected in the palea and carpel primordia (Figure 7B). Later, Sb AGL6 is still expressed in palea and gynoecium and is also detectable in lodicules (Figures 7C to 7E). Finally, expression is only detectable in the inner integument of the ovule (Figure 7F).
S. italica (Panicoideae) inflorescences bear pedicellate spikelets, each subtended by one to several undifferentiated branches (bristles; Doust and Kellogg, 2002 ). Each spikelet has an upper complete floret and a lower reduced floret. Si AGL6 was first detected in both floral meristems (Figure 8A
). Later, the gene is expressed in palea, lodicules, and carpel primordia (Figures 8B to 8F). Si AGL6 is on in the lower floral meristem even late in development (when all floral organs of the upper floret were initiated) even though no floral organs will form (Figure 8E). Finally, as in other species, late expression is restricted to the inner integument of the ovule of the upper floret (Figure 8F).
Reconstruction of the ancestral expression pattern estimates that the ancestral AGL6-like gene was expressed in the lodicules (inner tepals), stamens, and carpels but not in the glumes, lemma, or palea (Figure 9 ). This ancestral condition was maintained in S. angustifolia after which the expression in palea was gained in the rest of the grasses. Also, expression in the gynoecium was lost once in Os MADS17, and expression in stamens was independently lost twice (in the Bambusoideae + Pooideae and in the PACCMAD clades).
Sequence Evolution of AGL6-like Genes in Poales Our data on the timing of the rice MADS6/MADS17 duplication are contradictory. Phylogenetic analysis of AGL6-like genes in Poales indicates an ancient duplication event, giving rise to the paralogous clades of genes. Placement of the MADS17 clade after the divergence of Restionaceae and before that of Joinvilleaceae suggests that the duplication occurred before the common ancestor of the grasses and Joinvilleaceae, but we cannot reject the hypothesis of a duplication event just after the divergence of Joinvilleaceae, in the common ancestor of the grasses. The latter placement of the duplication is consistent with the ample evidence indicating a whole-genome duplication that characterizes all grasses, but likely not Joinvillea (Kellogg and Bennetzen, 2004 ; Kellogg, 2006). If the AGL6/MADS6 and MADS17 duplication reflects the whole-genome duplication of the grasses, we would expect to find orthologs of MADS17 in all grasses. We were therefore surprised that we could not find sequences homologous to MADS17 outside the genus Oryza. Our phylogeny implies that, after the duplication, MADS17 was lost multiple times and has been retained only in Oryza.
In contrast with the phylogenetic data, presence/absence data of MADS17 suggest that the duplication occurred before the diversification of Oryza. The hypothesis is also supported by the positions of MADS6 and MADS17 on rice chromosomes 2 and 4, respectively (coordinates 27870242-27877829 and 29123231-29128740; http://rice.plantbiology.msu.edu/cgi-bin/gbrowse/rice), in duplicated segments of the genome. This genomic duplication event may be unique to Oryza (http://www.tigr.org/tdb/e2k1/osa1/segmental_dup/500kb/segdup_500kb.shtml; see also Arora et al., 2007
Sequences from zag3 and zag5 duplicate genes formed two clades within Zea-Tripsacum, supporting the idea that zag3/zag5 were duplicates in the tetraploidy event preceding the Zea-Tripsacum divergence (Gaut and Doebley, 1997
Although selection among AGL6-like genes varies, we found no evidence for positive selection among sites. Our data are consistent with the structure of the MIKC MADS box genes, in which different regions of the genes are under different selective pressures (Becker and Theissen, 2003
Expression of AGL6-like Genes in Floral Meristems May Indicate a Role in Floral Meristem Identity
AGL6 mRNA was first detected in floral meristems in all grasses examined, even in floral meristems that never form floral organs, such as those in the sterile florets of Setaria and Sorghum. This result agrees with the loss-of-function mutant reported in maize (Thompson et al., 2009
In non-Poales monocots and in eudicots, mRNA of AGL6 orthologs is also detected in floral meristems prior to floral organ formation (Boss et al., 2002
AGL6-like Genes Are Markers for the Palea in Grasses
Most genes expressed in the palea are also expressed in the lemma, giving no clue how the two organs might be differentiated (Jeon et al., 2000
Our data show that AGL6-like genes could be another player in establishing palea development because expression in the developing palea is conserved among all spikelet-bearing grasses. Interestingly, no expression was identified in the bracts of S. angustifolia that have been thought to be homologous to the palea (Sajo et al., 2008
In addition to AGL6-like genes, LHS1 and FUL1/2 are also expressed in the palea (Malcomber and Kellogg, 2004
AGL6-like Genes May Have Been Involved in Inner Perianth Whorl Evolution during Angiosperm Diversification AGL6-like gene expression is conserved in the second whorl in grasses as well as in close relatives. Aaf AGL6 (A. africanus) and Ja AGL6 (J. ascendens) mRNA was detected in the inner tepals. In S. angustifolia, Sa AGL6 mRNA was detected in the bracts representing the inner whorl. In the rest of the grasses examined, AGL6-like mRNA was detected in lodicules. These results, together with functional data and previous expression analysis showing heterogeneous expression patterns in perianth whorls, suggest that perhaps AGL6-like genes may control some aspects of inner perianth formation and evolution.
AGL6-like Expression Is Conserved in Carpel Development and Ovule Formation but Not in Stamens
The expression and function of AGL6-like genes in carpel and ovule development can be traced back to the gymnosperms. In situ hybridization in Pinus radiata has shown that the AGL6 homologs Pr MADS2 and Pr MADS3 are expressed strongly in developing ovuliferous scale primordia and in the ovule (Mouradov et al., 1998
By contrast, expression of AGL6-like genes is not conserved during stamen development. Expression in microsporangia was detected in gymnosperms as well as in several angiosperms but not in all (Ma et al., 1991
Divergent Expression Patterns of Rice MADS6 and MADS17
We hypothesize that MADS17 may have different interacting partners than MADS6 because of the substantial differences in the C terminus. The C terminus of MADS box proteins is known to be essential for protein–protein interaction and transcriptional activation (Egea-Cortines et al., 1999 In summary, our comparative data show that the AGL6-like genes have multiple expression patterns that have originated at different evolutionary times; the fact that these expression domains originated millions of years apart suggests (but does not prove) that they each represent distinct developmental roles for the proteins. Gene expression during carpel development is likely as old as the seed plants themselves, whereas the expression in meristems and apparent functional role in meristem determinacy may be angiosperm specific. The proteins are presumably deployed in floral organ identity in different ways and at different times in angiosperm evolution, as indicated by variable expression patterns in stamens and outer and inner perianth whorls. Deployment of AGL6-like in the inner perianth whorl is shared among the grasses and their immediate relatives, whereas only the grasses express AGL6-like in the outer whorl. In the latter case, the novel gene expression pattern correlates with a highly modified and novel floral organ, the grass palea.
Sequencing and Phylogenetic Analyses Selection of species was based on phylogenetic position and variation in spikelet and flower morphology. Plants were grown in the greenhouse at the University of Missouri–St. Louis or the Missouri Botanical Garden.
A pool of MADS box cDNAs was produced following methods of Malcomber and Kellogg (2004)
Sequences were aligned using MUSCLE (Edgar, 2004a
Os MADS17-like Sequences To investigate syntenic regions in the rice and maize (Zea mays) genomes, we used the coordinates of MADS17 (Chr4:29082088..29102087) in the rice genome displayed at Gramene (http://www.gramene.org) and the maize genome displayed in (1) Gramene, (2) the maize genome sequence browser (http://maizesequence.org), and (3) Synteny (http://synteny.cnr.berkeley.edu/CoGe/.Read:Lyons).
Statistical Tests of Sequences
Characterization of Expression We also performed RT-PCR using specific primers designed to bind the 5' C terminus of the coding region and the 3' UTR (see Supplemental Table 4 online), except for Phalaris canariensis, Eragrostis tef, and Megathyrsus maximus, in which primers bind the 5' end of the I box and the 3' end of the C terminus. The RT reaction was performed using Superscript One-Step RT-PCR with Platinum Taq (Invitrogen) as per the manufacturer's instructions. ACTIN was used as a positive control.
For in situ hybridization, young inflorescences in different stages of development were dissected, fixed, and dehydrated as described by Malcomber and Kellogg (2004)
DNA Gel Blot Hybridization
Maximum Parsimony Ancestral State Reconstructions
Accession Numbers
Supplemental Data
We thank the Missouri Botanical Garden and the USDA for access to plant materials; Kenneth Olsen, Briana Gross, Pu Huang, and Barbara Schaal for access to Oryza material; Sarah Youngstrom for help with subcloning; Jinshun Zhong for help with RNA extractions; Simon Malcomber for assistance with in situ hybridizations; Xuemin (Sam) Wang, Liang Guo, and Geliang Wang for assistance with real time Q-PCR; and Simon Malcomber and Felipe Zapata for assistance and helpful discussions. We are also indebted to Simon Malcomber and Ashley Christensen for the unpublished sequence of Elegia and Sarah Hake, Beth Thompson, and members of the Kellogg lab for critical reading of the manuscript. This work was funded by National Science Foundation Grant DBI-0604923 to E.A.K.
The authors responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) are: Renata Reinheimer (reinheimerr{at}umsl.edu) and Elizabeth A. Kellogg (kellogge{at}umsl.edu).
[W] Online version contains Web-only data.
[OA] Open access articles can be viewed online without a subscription. www.plantcell.org/cgi/doi/10.1105/tpc.109.068239 Received April 26, 2009; Revision received August 10, 2009. accepted August 25, 2009.
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ABSTRACT
INTRODUCTION
T; black arrow in Supplemental Figure 2 online) changed before the divergence of Pharus and has been unchanged ever since; this correlates with the origin of the grass spikelet (
values from 0.01390 [purifying selection] to 0.72797 [relaxed selection]). We found no evidence of positive selection; none of the AGL6-like sequences have overall 
