Divergent Expression Patterns of miR164 and CUP-SHAPED COTYLEDON Genes in Palms and Other Monocots: Implication for the Evolution of Meristem Function in Angiosperms

H Adam,F Richaud,P Laufs,M Collin,J W Tregear,Y Vigouroux,R Qadri,A.-C Thuillet,B Adroher,S Jouannic,M Marguerettaz

doi:10.1093/molbev/msq328

Abstract

In order to understand how the morphology of plant species has diversified over time, it is necessary to decipher how the underlying developmental programs have evolved. The regulatory network controlling shoot meristem activity is likely to have played an important role in morphological diversification and useful insights can be gained by comparing monocots and eudicots. These two distinct monophyletic groups of angiosperms diverged 130 Ma and are characterized by important differences in their morphology. Several studies of eudicot species have revealed a conserved role for NAM and CUC3 genes in meristem functioning and pattern formation through the definition of morphogenetic boundaries during development. In this study, we show that NAM- and CUC3-related genes are conserved in palms and grasses, their diversification having predated the radiation of monocots and eudicots. Moreover, the NAM-miR164 posttranscriptional regulatory module is also conserved in palm species. However, in contrast to the CUC3-related genes, which share a similar expression pattern between the two angiosperm groups, the expression domain of the NAM-miR164 module differs between monocot and eudicot species. In our studies of spatial expression patterns, we compared existing eudicot data with novel results from our work using two palm species (date palm and oil palm) and two members of the Poaceae (rice and millet). In addition to contrasting results obtained at the gene expression level, major differences were also observed between eudicot and monocot NAM-related genes in the occurrence of putative cis-regulatory elements in their promoter sequences. Overall, our results suggest that although NAM- and CUC3-related proteins are functionally equivalent between monocots and eudicots, evolutionary radiation has resulted in heterotopy through alterations in the expression domain of the NAM-miR164 regulatory module.

Highlights

Angiosperm species display an enormous diversity in their architecture and in the structure of their individual organs
The NAM-related genes are expressed within the spikelet and floral meristems and not in the M-O and floral O-O boundaries (Zimmerman and Werr 2005). These results suggest that the NAM/CUC3 genes from maize and rice may be partially divergent in their function compared with the situation in eudicots
Blast analyses revealed that the deduced EgNAM1 and PdNAM1 polypeptides were related to the proteins AtCUC1 and AtCUC2 from A. thaliana, whereas EgCUC3 and PdCUC3 were more related to the A. thaliana AtCUC3 protein

Summary

Introduction

Angiosperm species display an enormous diversity in their architecture and in the structure of their individual organs. One of the most important evolutionary questions is to understand how this morphological diversity arises during evolution. In order to understand how angiosperm morphology has radiated during evolution, it is interesting to investigate how meristem function has diverged between different groups. One important morphological dichotomy observed during angiosperm evolution is the split between the monocots and eudicots lineages, which diverged 130 Ma. In angiosperms, the shoot meristem is typically a domeshaped structure with a characteristic inner organization of tissues, containing a group of undifferentiated and dividing cells (Kwiatkowska 2008). The formation of an organ primordium without disrupting the integrity of the meristem requires the creation of boundaries that separate the primordium from surrounding tissues, in order to delineate territories, which will undergo different cell fates

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