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


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
12 2019
Historique:
received: 07 07 2019
accepted: 11 11 2019
entrez: 10 12 2019
pubmed: 10 12 2019
medline: 21 3 2020
Statut: epublish

Résumé

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.

Identifiants

pubmed: 31815938
doi: 10.1371/journal.pbio.3000560
pii: PBIOLOGY-D-19-01942
pmc: PMC6901180
doi:

Substances chimiques

Plant Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3000560

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Satoshi Naramoto (S)

Graduate School of Life Sciences, Tohoku University, Sendai, Japan.

Victor Arnold Shivas Jones (VAS)

Department of Plant Sciences, University of Oxford, Oxford, United Kingdom.

Nicola Trozzi (N)

Graduate School of Life Sciences, Tohoku University, Sendai, Japan.
Department of Molecular Biology, Umeå University, Umeå, Sweden.

Mayuko Sato (M)

RIKEN Center for Sustainable Resource Science, Yokohama, Japan.

Kiminori Toyooka (K)

RIKEN Center for Sustainable Resource Science, Yokohama, Japan.

Masaki Shimamura (M)

Graduate School of Integrated Sciences for life, Hiroshima University, Higashi-Hiroshima, Japan.

Sakiko Ishida (S)

Graduate School of Biostudies, Kyoto University, Kyoto, Japan.

Kazuhiko Nishitani (K)

Department of Biological Sciences, Kanagawa University, Hiratsuka, Japan.

Kimitsune Ishizaki (K)

Graduate School of Science, Kobe University, Kobe, Japan.

Ryuichi Nishihama (R)

Graduate School of Biostudies, Kyoto University, Kyoto, Japan.

Takayuki Kohchi (T)

Graduate School of Biostudies, Kyoto University, Kyoto, Japan.

Liam Dolan (L)

Department of Plant Sciences, University of Oxford, Oxford, United Kingdom.

Junko Kyozuka (J)

Graduate School of Life Sciences, Tohoku University, Sendai, Japan.

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Classifications MeSH