The cellular function of ROP GTPase prenylation is important for multicellularity in the moss Physcomitrium patens

被引:9
作者
Bao, Liang [1 ,6 ]
Ren, Junling [1 ,6 ]
Nguyen, Mary [1 ]
Slusarczyk, Arkadiusz Slawomir [2 ]
Thole, Julie M. [3 ]
Martinez, Susana Perez [1 ]
Huang, Jinling [4 ]
Fujita, Tomomichi [5 ]
Running, Mark P. [1 ]
机构
[1] Univ Louisville, Dept Biol, Louisville, KY 40208 USA
[2] Univ Louisville, Dept Anat Sci & Neurobiol, Louisville, KY 40202 USA
[3] St Louis Univ, Dept Biol, St Louis, MO 63103 USA
[4] East Carolina Univ, Dept Biol, Greenville, NC 27858 USA
[5] Hokkaido Univ, Fac Sci, Sapporo, Hokkaido 0600810, Japan
[6] Virginia Commonwealth Univ, Philips Inst Oral Hlth Res, Richmond, VA 23298 USA
来源
DEVELOPMENT | 2022年 / 149卷 / 12期
基金
美国国家科学基金会;
关键词
Protein prenylation; ROP GTPase; Evolution; Land plants; Unicellular; Multicellularity; Cell expansion; Cell wall integrity; 3D GROWTH TRANSITION; TIP GROWTH; ARTIFICIAL MICRORNAS; ACTIN DYNAMICS; RHO; ADHESION; ORIGINS; DIFFERENTIATION; DIVISION; FAMILY;
D O I
10.1242/dev.200279
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
A complete picture of how signaling pathways lead to multicellularity is largely unknown. Previously, we generated mutations in a protein prenylation enzyme, GGB, and showed that it is essential for maintaining multicellularity in the moss Physcomitrium patens. Here, we show that ROP GTPases act as downstream factors that are prenylated by GGB and themselves play an important role in the multicellularity of P. patens. We also show that the loss of multicellularity caused by the suppression of GGB or ROP GTPases is due to uncoordinated cell expansion, defects in cellwall integrity and the disturbance of the directional control of cell plate orientation. Expressing prenylatable ROP in the ggb mutant not only rescues multicellularity in protonemata but also results in development of gametophores. Although the prenylation of ROP is important for multicellularity, a higher threshold of active ROP is required for gametophore development. Thus, our results suggest that ROP activation via prenylation by GGB is a key process at both cell and tissue levels, facilitating the developmental transition from one dimension to two dimensions and to three dimensions in P. patens.
引用
收藏
页数:9
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共 51 条
[1]   Diverse evolutionary paths to cell adhesion [J].
Abedin, Monika ;
King, Nicole .
TRENDS IN CELL BIOLOGY, 2010, 20 (12) :734-742
[2]   Turning moss into algae Prenylation targets in Physcomitrella patens [J].
Antimisiaris, Marika F. ;
Running, Mark P. .
PLANT SIGNALING & BEHAVIOR, 2014, 9 (07)
[3]   AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens [J].
Aoyama, Tsuyoshi ;
Hiwatashi, Yuji ;
Shigyo, Mikao ;
Kofuji, Rumiko ;
Kubo, Minoru ;
Ito, Motomi ;
Hasebe, Mitsuyasu .
DEVELOPMENT, 2012, 139 (17) :3120-3129
[4]   The Origin of Animal Multicellularity and Cell Differentiation [J].
Brunet, Thibaut ;
King, Nicole .
DEVELOPMENTAL CELL, 2017, 43 (02) :124-140
[5]   A family of ROP proteins that suppresses actin dynamics, and is essential for polarized growth and cell adhesion [J].
Burkart, Graham M. ;
Baskin, Tobias I. ;
Bezanilla, Magdalena .
JOURNAL OF CELL SCIENCE, 2015, 128 (14) :2553-2564
[6]   Origin of animal multicellularity: precursors, causes, consequences-the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion [J].
Cavalier-Smith, Thomas .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2017, 372 (1713)
[7]   A Fully Functional ROP Fluorescent Fusion Protein Reveals Roles for This GTPase in Subcellular and Tissue-Level Patterning[OPEN] [J].
Cheng, Xiaohang ;
Mwaura, Bethany W. ;
Chang Stauffer, Sophia R. ;
Bezanilla, Magdalena .
PLANT CELL, 2020, 32 (11) :3436-3451
[8]   Mosses as model systems for the study of metabolism and development [J].
Cove, David ;
Bezanilla, Magdalena ;
Harries, Phillip ;
Quatrano, Ralph .
ANNUAL REVIEW OF PLANT BIOLOGY, 2006, 57 :497-520
[9]   Protein isoprenylation: the fat of the matter [J].
Crowell, Dring N. ;
Huizinga, David H. .
TRENDS IN PLANT SCIENCE, 2009, 14 (03) :163-170
[10]   Physcomitrella patens: a model to investigate the role of RAC/ROP GTPase signalling in tip growth [J].
Eklund, D. Magnus ;
Svensson, Emma M. ;
Kost, Benedikt .
JOURNAL OF EXPERIMENTAL BOTANY, 2010, 61 (07) :1917-1937