A conserved regulatory mechanism mediates the convergent evolution of plant shoot lateral organs.

Satoshi Naramoto,Nicola Trozzi,Junko Kyozuka,Kiminori Toyooka,Kimitsune Ishizaki,Takayuki Kohchi,Kazuhiko Nishitani,Liam Dolan,Masaki Shimamura,Victor Arnold Shivas Jones,Ryuichi Nishihama,Sakiko Ishida,Mayuko Sato,Mark Estelle

doi:10.1371/journal.pbio.3000560

Abstract

Land plant shoot structures evolved a diversity of lateral organs as morphological adaptations to the terrestrial environment, with lateral organs arising independently in different lineages. Vascular plants and bryophytes (basally diverging land plants) develop lateral organs from meristems of sporophytes and gametophytes, respectively. Understanding the mechanisms of lateral organ development among divergent plant lineages is crucial for understanding the evolutionary process of morphological diversification of land plants. However, our current knowledge of lateral organ differentiation mechanisms comes almost entirely from studies of seed plants, and thus, it remains unclear how these lateral structures evolved and whether common regulatory mechanisms control the development of analogous lateral organs. Here, we performed a mutant screen in the liverwort Marchantia polymorpha, a bryophyte, which produces gametophyte axes with nonphotosynthetic scalelike lateral organs. We found that an Arabidopsis LIGHT-DEPENDENT SHORT HYPOCOTYLS 1 and Oryza G1 (ALOG) family protein, named M. polymorpha LATERAL ORGAN SUPRESSOR 1 (MpLOS1), regulates meristem maintenance and lateral organ development in Marchantia. A mutation in MpLOS1, preferentially expressed in lateral organs, induces lateral organs with misspecified identity and increased cell number and, furthermore, causes defects in apical meristem maintenance. Remarkably, MpLOS1 expression rescued the elongated spikelet phenotype of a MpLOS1 homolog in rice. This suggests that ALOG genes regulate the development of lateral organs in both gametophyte and sporophyte shoots by repressing cell divisions. We propose that the recruitment of ALOG-mediated growth repression was in part responsible for the convergent evolution of independently evolved lateral organs among highly divergent plant lineages, contributing to the morphological diversification of land plants.

Highlights

During 470 million years of evolution, the body plans of land plants diversified independently among the gametophyte and sporophyte life stages of different plant groups
In addition to the abnormal green outgrowths, gemma cup spacing was abnormal in the Mplos1-1 mutant; the distance between neighboring gemma cups was much shorter than in the wild type (WT) (Fig 1F and 1G)
We demonstrate that MpLOS1, a member of the Arabidopsis LIGHTDEPENDENT SHORT HYPOCOTYLS 1 (LSH1) and Oryza long sterile lemma (G1) (ALOG) gene family, plays a role in integrating meristem activity and lateral organ differentiation in M. polymorpha

Summary

Introduction

During 470 million years of evolution, the body plans of land plants diversified independently among the gametophyte and sporophyte life stages of different plant groups. Early-diverging land plants, the gametophyte is the dominant phase of the life cycle [1,2]. The gametophyte comprises an apical–basal axis with an apical stem cell and forms structures in which gametes develop (antheridiophores and archegoniophores). The sporophyte is dominant in extant vascular plants. The sporophyte comprises an axial system (shoots or stems growing along apical–basal axes) that develops from an apical meristem and forms structures in which haploid spores develop. In different plant lineages, gametophytes and sporophytes develop axial systems that are produced by apical meristems [3,4,5]

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Conclusion