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

PLoS Biol. 2019 Dec 9;17(12):e3000560. doi: 10.1371/journal.pbio.3000560. eCollection 2019 Dec.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis / genetics
  • Biological Evolution
  • Evolution, Molecular
  • Gene Expression Regulation, Plant / genetics
  • Meristem / genetics
  • Meristem / growth & development
  • Meristem / metabolism*
  • Oryza / genetics
  • Phenotype
  • Phylogeny
  • Plant Proteins / metabolism
  • Plant Shoots / genetics*
  • Plant Shoots / growth & development
  • Plant Shoots / metabolism*
  • Plants / genetics
  • Plants, Genetically Modified / metabolism

Substances

  • Plant Proteins

Grants and funding

The funders of this research are the Grants-in-Aid from the Ministry of Education, Culture, Sports and Technology, Japan (https://www.jsps.go.jp/english/e-grants/) (KAKENHI grant numbers 17K17595 for SN, 18H04836 for RN, 17H06472 for KI, and 17H06465 for JK); Newton Abraham Studentship from the University of Oxford, to VASJ; and ERC advanced Grant EVO-500 (250284) (https://erc.europa.eu/funding/advanced-grants) to LD. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.