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

Abstract

The morphological variation among reproductive organs of extant gymnosperms is remarkable, especially among conifers. Several hypotheses concerning morphological homology between various conifer reproductive organs have been put forward, in particular in relation to the pine ovuliferous scale. Here, we use the expression patterns of orthologs of the ABC-model MADS-box gene AGAMOUS (AG) for testing morphological homology hypotheses related to organs of the conifer female cone. To this end, we first developed a tailored 3'RACE procedure that allows reliable amplification of partial sequences highly similar to gymnosperm-derived members of the AG-subfamily of MADS-box genes. Expression patterns of two novel conifer AG orthologs cloned with this procedure-namely PodAG and TgAG, obtained from the podocarp Podocarpus reichei and the yew Taxus globosa, respectively-are then further characterized in the morphologically divergent female cones of these species. The expression patterns of PodAG and TgAG are compared with those of DAL2, a previously discovered Picea abies (Pinaceae) AG ortholog. By treating the expression patterns of DAL2, PodAG, and TgAG as character states mapped onto currently accepted cladogram topologies, we suggest that the epimatium-that is, the podocarp female cone organ previously postulated as a "modified" ovuliferous scale-and the canonical Pinaceae ovuliferous scale can be legitimally conceptualized as "primary homologs." Character state mapping for TgAG suggests in turn that the aril of Taxaceae should be considered as a different type of organ. This work demonstrates how the interaction between developmental-genetic data and formal cladistic theory could fruitfully contribute to gymnosperm systematics.

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

“…Specifically, our data indicate that CjMADS4, TdMADS3, and JcMADS2 are the orthologs in each respective species both to each other and to DAL2 and SAG1 in Picea abies and Picea mariana, respectively. Our data further indicate that these genes are orthologous to PodAG and TgAG (Englund et al 2011), in the conifer families Podocarpaceae and Taxaceae, respectively. We cannot exclude the possibility that in one or more of these conifer species there are AG subfamily genes paralogous to the gene presented here present in the genome.…”

“…TdMADS3, JcMADS2, and CjMADS4 all belong to the conifer section of the AG clade, together with the Picea protein DAL2. Sequences for the conifer genes PodAG ( Podocarpus reichei ) and TgAG ( Taxus globosa ) are characterized in more detail in Englund et al (2011). For accession numbers of all proteins included in the analysis, see supporting information Table S2.…”

“…4, J and K), but no CjMADS4 expression was observed in any other parts of the expanding tooth. In mature cones, the positions of the and TgAG (Taxus globosa) are characterized in more detail in Englund et al (2011). For accession numbers of all proteins included in the analysis, see supporting information Table S2.…”

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

“…We found that DAL2 was expressed throughout the nucellus and the outer cell layers of the integument (Fig. e,i,k; Englund et al ., ), whereas DAL14 expression was detected throughout the integument, but not in the nucellus (Fig. f,j,l).…”

“…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.…”