Why are orchid flowers so diverse? Reduction of evolutionary constraints by paralogues of class B floral homeotic genes

Abstract

The four DEF paralogues shaped floral diversity in orchids in a dramatic way by modularizing the floral perianth based on a complex series of sub- and neo-functionalization events. These genes may have eliminated constraints, so that different kinds of perianth organs could then evolve individually and thus often in dramatically different ways in response to selection by pollinators or by genetic drift. We therefore argue that floral diversity in orchids may be the result of an unprecedented developmental genetic predisposition that originated early in orchid evolution.

Conserved differential expression of paralogous DEFICIENS‐ and GLOBOSA‐like MADS‐box genes in the flowers of Orchidaceae: refining the ‘orchid code’

“…Previously, we linked the pattern of expression of DEF-like genes, documented by analyses of wild-type and perianthmutant (peloric) orchids (Hsu and Yang, 2002;Tsai et al, 2004;Xu et al, 2006;Kim et al, 2007), with data that we had generated on the molecular phylogeny of these genes (Mondragó n-Palomino and Theißen, 2008Theißen, , 2009. We found that DEF-like genes of orchids are grouped into four wellsupported ancient clades (Figure 1b), and that genes from a specific clade are expressed in the same organs of the perianth.…”

“…Specifically, genes from clade 1 (PeMADS2-like genes) and clade 2 (OMADS3-like genes) are expressed in all tepals (Hsu and Yang, 2002;Tsai et al, 2004;Xu et al, 2006), whereas genes from clade 3 (PeMADS3-like genes) are only expressed in inner tepals (Tsai et al, 2004;Xu et al, 2006;Kim et al, 2007), and genes from clade 4 (PeMADS4-like genes) are exclusively expressed in the labellum (Tsai et al, 2004). This suggested a simple combinatorial model for organ identity specification that we termed the 'orchid code' (Mondragó n-Palomino and Theißen, 2008Theißen, , 2009). Assuming (e) The expression of class-B genes was also analyzed in the organs of both wild-type and peloric buds of the Phalaenopsis hybrid 'Athens'.…”

“…According to our hypothesis, the difference between outer and inner tepals depends on the differential expression of clade-3 genes. Similarly, the distinction between inner lateral tepals and the labellum is determined by differential expression of clade-4 genes (Mondragó n-Palomino and Theißen, 2008Theißen, , 2009.…”

“…Previously, the orchid code hypothesis considered only the presence or absence of the expression of class-B genes in specific perianth organs (Figure 6b; Mondragó nPalomino and Theißen, 2008Theißen, , 2009). However, the experi-mental analyses outlined here (summarized in Figure 6a) instead suggest a model, the 'refined orchid code', in which the relative levels of expression are key to the development of specific structures (Figure 6c).…”

“…Mutations and natural selection on specific genes or their targets would affect individual modules without changing the rest of the flower, and thus facilitated the spectacular morphological diversification of the orchid labellum (Mondragó n-Palomino and Theißen, 2009). This also holds in the revised model.…”