MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes

Abstract

MADS-box genes encode transcriptional regulators involved in diverse aspects of plant development. Here we describe the cloning and mRNA spatio-temporal expression patterns of five new MADS-box genes from Arabidopsis: AGL16, AGL18, AGL19, AGL27 and AGL31. These genes will probably become important molecular tools for both evolutionary and functional analyses of vegetative structures. We mapped our data and previous expression patterns onto a new MADS-box phylogeny. These analyses suggest that the evolution of the MADS-box family has involved a rapid and simultaneous functional diversification in vegetative as well as reproductive structures. The hypothetical ancestral genes had broader expression patterns than more derived ones, which have been co-opted for putative specialized functions as suggested by their expression patterns. AGL27 and AGL31, which are closely related to the recently described flowering-time gene FLC (previously AGL25), are expressed in most plant tissues. AGL19 is specifically expressed in the outer layers of the root meristem (lateral root cap and epidermis) and in the central cylinder cells of mature roots. AGL18, which is most similar in sequence to the embryo-expressed AGL15 gene, is expressed in the endosperm and in developing male and female gametophytes, suggesting a role for AGL18 that is distinct from previously characterized MADS-box genes. Finally, AGL16 RNA accumulates in leaf guard cells and trichomes. Our new phylogeny reveals seven new monophyletic clades of MADS-box sequences not specific to flowers, suggesting that complex regulatory networks involving several MADS-box genes, similar to those that control flower development, underlie development of vegetative structures.

Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny

“…Another important finding is the strong association of AGL79, expressed in roots (data not shown), with AP1, CAL, and FUL, which are well characterized flower development genes (43). Therefore, this tree suggests that not all monophyletic groups resolved include genes with similar expression patterns and functions as previously thought (15,21), but formal and robust inferences on evolution of MADS-box gene expression and function will have to await more experimental data and the inclusion of genes from additional taxa.…”

“…All but one (16) functionally characterized plant MADS-box genes are type II and encode the three floral homeotic functions of the flower development ABC model (17-19). They also encode regulators of flower initiation, flower meristem identity, and various aspects of ovule, fruit, leaf, and root development (11,(20)(21)(22)(23). All characterized plant type II MADS-box genes encode proteins that share a stereotypical MIKC structure, with highly conserved MADS and K domains that are putative DNA-binding and protein-protein interaction domains, respectively, and less conserved I and COOH regions.…”

miR824-Regulated AGAMOUS-LIKE16 Contributes to Flowering Time Repression in Arabidopsis

“…miR824 is expressed in many tissues including rosette and cauline leaves, shoots, inflorescences, and roots (Kutter et al, 2007). The expression of AGL16, the only confirmed target for miR824, is also detected in these tissues as well as in guard cells, trichomes, and developing siliques (Alvarez-Buylla et al, 2000). In agreement with its expression in guard cells, the miR824/AGL16 module was shown to regulate the development of higher-order stomata complexes by promoting additional divisions of satellite meristemoid cells (Kutter et al, 2007).…”

Genome-wide identification of MADS-box family genes in moso bamboo (Phyllostachys edulis) and a functional analysis of PeMADS5 in flowering

“…MADS-box genes encode a large family of transcription factors that have essential roles in animals, plants, and fungi [1]. The first plant MADS-box genes were found to regulate floral meristem identity.…”