Genetic Footprints of Stamen Ancestors Guide Perianth Evolution inPersea(Lauraceae)

Abstract

The perianth of Persea americana, like that of most Lauraceae, consists of two whorls of morphologically similar petaloid organs, termed tepals. In closely related Persea borbonia however, a sepaloid outer whorl of tepals contributes to a dimorphic perianth. To determine whether Persea homologues of the A-, B-, C-, and E-class MADS-box genes that determine organ identity in eudicot flowers have played a role in shaping this dimorphic perianth, their expression levels were assessed across the floral whorls of P. americana and P. borbonia. We find that homologues of A-and B-function genes from Persea are expressed at comparable levels in the perianth whorls of the two species, but homologues of AG (C-function) and SEP3 (E-function) have shifted away from sepaloid tepals of Persea borbonia. Genetic studies suggest a conserved role for AG homologues in specifying stamen and carpel identity in Persea, but the coincidence of phenotypic and gene expression shifts argues for a hitherto unprecedented role in perianth development. Phylogenetic conservation of SEP3-AG interaction in floral organ identity transcription factor quartets may underlie the coincident shift of Persea AG and SEP3 gene expression. Based on our results, we hypothesize: 1) A role for Persea AG and SEP3 homologues in shaping perianth morphology is indicated by the coincident shift to a dimorphic perianth with loss of their expression in the outer tepals of Persea borbonia. 2) Reproductive organ identity in Persea is specified through the action of three AG homologues. 3) The expression of floral organ identity homologues in the tepals of Persea, and perhaps other Lauraceae, is suggestive of staminal origin, i.e., andropetals.

Evolution ofAGL6-likeMADS Box Genes in Grasses (Poaceae): Ovule Expression Is Ancient and Palea Expression Is New

“…Similar results have been obtained in zag3 in situ hybridization and, moreover, zag3 mutants produce extra carpels in the ear (Thompson et al, 2009). These data are consistent with many other studies that have detected expression in carpels and ovules in angiosperms (Ma et al, 1991;Mena et al, 1995;Rounsley et al, 1995;Moon et al,1999;Tsuchimoto et al, 2000;Boss et al, 2002;Pelucchi et al, 2002;Hsu et al, 2003;Losa et al, 2004;Petersen et al, 2004;Chanderbali et al, 2006;Fan et al, 2007), except in Persea and Magnolia where RT-PCR failed to detect AGL6 expression in the carpel . Curiously, yeast two-hybrid data fail to show any interaction of AGL6-like proteins with B and C class MADS box proteins in rice (Moon et al, 1999), whereas the maize AGL6 homolog, ZAG3, does interact with the AG homolog, ZAG1 (Thompson et al, 2009).…”

“…Expression in microsporangia was detected in gymnosperms as well as in several angiosperms but not in all (Ma et al, 1991;Mena et al, 1995;Rounsley et al, 1995;Tandre et al, 1995;Liu and Podila, 1997;Mouradov et al, 1998;Moon et al,1999;Winter et al, 1999;Tsuchimoto et al, 2000;Boss et al, 2002;Pelucchi et al, 2002;Hsu et al, 2003;Losa et al, 2004;Petersen et al, 2004;Chanderbali et al, 2006;Fan et al, 2007). Our in situ hybridizations showed that AGL6-like genes are expressed in stamens only in J. ascendens, the grass S. angustifolia in Anomochlooideae, and in Ehrhartoideae.…”

“…AGL6-like genes are expressed exclusively in the second whorl in species that have flowers with novel structures such as the cap in Vitis vinifera (Boss et al, 2002) or the lip in Oncidium (Hsu et al, 2003); otherwise, AGL6 expression was detected in both whorl 1 and whorl 2 (Ma et al, 1991;Tsuchimoto et al, 2000;Losa et al, 2004;Kim et al, 2005;Chanderbali et al, 2006;Fan et al, 2007). In grasses, previous studies suggest that AGL6 orthologs are expressed in lodicules as well as in the palea (Mena et al, 1995;Moon et al, 1999;Aiguo and Griffin, 2002;Petersen et al, 2004;Thompson et al, 2009).…”

Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower

“…5). Homologs of organidentity genes also are broadly expressed during the initial stages of Nuphar and Persea floral development (12,30), when organ identity is thought to be specified, suggesting that the transcriptional patterns we find in their late-stage flowers also may characterize their early developmental programs.…”

“…Evolutionary reconstructions of expression patterns of key floral transcription factors show progressively more spatially restricted deployment throughout angiosperm evolution, from across the floral meristem in Amborella, Nuphar, and Persea, for example, to specific organs in Arabidopsis and other eudicots (12,30,31). Likewise, the transcriptional cascades that are broadly deployed in Nuphar and Persea have been tightly constrained spatially within organ-specific boundaries in Eschscholzia and Arabidopsis.…”