AGAMOUS subfamily MADS-box genes and the evolution of seed cone morphology in Cupressaceae and Taxodiaceae

Abstract

In this comparative developmental genetics study, we test hypotheses based on fossil and morphological data on reproductive organ morphology and evolution in conifers--specifically, the ovule-bearing organ in Cupressaceae and Taxodiaceae. Genes homologous to the Arabidopsis gene AGAMOUS are expressed in ovuliferous scales of spruces (Picea) throughout development. Previous studies have shown that the AGAMOUS subfamily of MADS-box genes predates the split between angiosperms and gymnosperms, and that these genes have in part conserved functions in reproductive development among seed plants, especially in the specification of identity of the ovule-bearing organs. These data indicate that their expression in conifer families other than Pinaceae might be used as markers for organs homologous to the Pinaceae ovuliferous scale. Here we have isolated putative AGAMOUS orthologs from Cupressaceae and Taxodiaceae and analyzed their expression pattern in seed cones to test for the presence of morphological homologs of ovuliferous scales. Our results were not congruent with the hypothesis that the tooth of the Cryptomeria seed cone is homologous to the Picea ovuliferous scale. Likewise, the hypothesis that the bracts of Thujopsis and Juniperus contain fused ovuliferous scales was not supported. However, we found expression of AGAMOUS homologs in the sterile bracts of Cupressaceae seed cones at late developmental stages. This expression probably represents a novel gene function in these conifer families, since no corresponding expression has been identified in Pinaceae. Our study suggests that the evolutionary history of modern conifer cones is more diverse than previously thought.

Morphological “primary homology” and expression of AG -subfamily MADS-box genes in pines, podocarps, and yews

“…We suggest that this result might be due to random higher similarities between GGM3, PodAG , and TgAG in the small matrix we analyzed. This suggestion is supported by the results presented in the accompanying paper by Groth et al (2011), where the matrix analyzed phylogenetically included a much larger sampling of AG ‐related sequences from gymnosperms as well as angiosperms. In their cladogram, Groth et al (2011) have found that GGM3 is sister branch of a clade composed exclusively by conifer sequences, as expected from the aforementioned molecular systematics works.…”

“…2), it can be observed that both PodAG and TgAG, and the four cycad genes CerAG, MacAG, StaAG, and ZamAG, contain recognizable versions of the AG Motifs I and II identified by Kramer et al (2004). A complementary cladistic analysis on a matrix of translated sequences including several additional AG-subfamily homologs from gymnospermsFincluding three new putative orthologs from Cupressaceae/Tax-odiaceaeFand angiosperms is presented in the accompanying paper by Groth et al (2011).…”

“…ovuliferous scale, epimatium, or aril). The matrix was then associated to a simplified phylogeny that includes Pinaceae, Podocarpaceae and Taxaceae as terminals, plus Cupressaceae (a family closely related to Taxaceae and the focus of the accompanying study by Groth et al 2011) and an ''outgroup'' branch. As a result of this coding, a set of relationships can easily be detected: (i) at an early stage, DAL2, PodAG and TgAG are all expressed in both ovular structures; (ii) the AG-subfamily gene in Picea and Podocarpus is expressed both early and late in the integument, but only early in Taxus; (iii) the AG-subfamily gene of Picea and Podocarpus is not expressed at late stages in the nucellus, but is present throughout in Taxus, and (iv) the expression pattern of the AG-subfamily gene in the Picea ovuliferous scale and the Podocarpus epimatium is similar (early presence, late absence), in contrast to an ''early absence-late presence'' pattern in the Taxus aril ( Fig.…”

Molecular control of normal and acrocona mutant seed cone development in Norway spruce (Picea abies) and the evolution of conifer ovule‐bearing organs

“…Transcription factors of the MADS-domain family play key roles in both processes, in addition to LEAFY (LFY), which acts as an initiator of the floral-organ identity MADS-box genes. The gymnosperm homologues to the MADS-box C-class genes, in angiosperms specifying carpel identity and, together with the B genes, stamen development, are all expressed in ovule-carrying and pollen-producing organs, whereas B-class homologues appear to be specific to the pollen-producing organs (Tandre et al, 1995(Tandre et al, , 1998Rutledge et al, 1998;Sundstr€ om et al, 1999;Winter et al, 1999;Sundstr€ om & Engstr€ om, 2002;Carlsbecker et al, 2003Carlsbecker et al, , 2004Jager et al, 2003;Zhang et al, 2004;V azquez-Lobo et al, 2007;Englund et al, 2011;Groth et al, 2011;Lovisetto et al, 2012). Hence, a substantial conservation of reproductive development control is apparent and implies that C-class homologues specify reproductive identity and B-class homologues distinguish male from female identity in all seed plant groups.…”

Distinct double flower varieties in Camellia japonica exhibit both expansion and contraction of C-class gene expression

“…More surprisingly, despite markedly petaloid shape, the late expression of C- function gene was detected in the corona of daffodil [19], which suggested that corona might have a stamen-like origin but with changes of developmental pathways that dictating morphogenesis [19]. AGAMOUS ( AG ) is the only C class gene in Arabidopsis and its function in many higher plants including monocots are highly conserved [20,21]. In Davidia involucrata , the bract organ resembled petals, yet expressions of both B- and C- function homologs were detected [22], suggesting that certain expression combinations of ABC genes may not be sufficient to specify expected floral organ identities.…”