Divergent functions of the myotubularin (MTM) homologs AtMTM1 and AtMTM2 in Arabidopsis thaliana: Evolution of the plant MTM family

Yong Ding, Ivan Ndamukong, Yang Zhao, Yuannan Xia, Jean Jack Riethoven, David R. Jones, Nullin Divecha, Zoya Avramova

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Myotubularin and myotubularin-related proteins are evolutionarily conserved in eukaryotes. Defects in their function result in muscular dystrophy, neuronal diseases and leukemia in humans. In contrast to the animal lineage, where genes encoding both active and inactive myotubularins (phosphoinositide 3-phosphatases) have appeared and proliferated in the basal metazoan group, myotubularin genes are not found in the unicellular relatives of green plants. However, they are present in land plants encoding proteins highly similar to the active metazoan enzymes. Despite their remarkable structural conservation, plant and animal myotubularins have significantly diverged in their functions. While loss of myotubularin function causes severe disease phenotypes in humans it is not essential for the cellular homeostasis under normal conditions in Arabidopsis thaliana. Instead, myotubularin deficiency is associated with altered tolerance to dehydration stress. The two Arabidopsis genes AtMTM1 and AtMTM2 have originated from a segmental chromosomal duplication and encode catalytically active enzymes. However, only AtMTM1 is involved in elevating the cellular level of phosphatidylinositol 5-phosphate in response to dehydration stress, and the two myotubularins differentially affect the Arabidopsis dehydration stress-responding transcriptome. AtMTM1 and AtMTM2 display different localization patterns in the cell, consistent with the idea that they associate with different membranes to perform specific functions. A single amino acid mutation in AtMTM2 (L250W) results in a dramatic loss of subcellular localization. Mutations in this region are linked to disease conditions in humans.

Original languageEnglish (US)
Pages (from-to)866-878
Number of pages13
JournalPlant Journal
Volume70
Issue number5
DOIs
StatePublished - Jun 1 2012

Fingerprint

Arabidopsis
Arabidopsis thaliana
mutation
conservation plants
muscular dystrophy
genes
Dehydration
phosphatidylinositols
embryophytes
plant proteins
enzymes
leukemia
transcriptome
eukaryotic cells
homeostasis
animals
phosphates
phenotype
amino acids
Genomic Segmental Duplications

Keywords

  • Arabidopsis MTM1
  • MTM2
  • evolution
  • plant myotubularins

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Divergent functions of the myotubularin (MTM) homologs AtMTM1 and AtMTM2 in Arabidopsis thaliana : Evolution of the plant MTM family. / Ding, Yong; Ndamukong, Ivan; Zhao, Yang; Xia, Yuannan; Riethoven, Jean Jack; Jones, David R.; Divecha, Nullin; Avramova, Zoya.

In: Plant Journal, Vol. 70, No. 5, 01.06.2012, p. 866-878.

Research output: Contribution to journalArticle

Ding, Yong ; Ndamukong, Ivan ; Zhao, Yang ; Xia, Yuannan ; Riethoven, Jean Jack ; Jones, David R. ; Divecha, Nullin ; Avramova, Zoya. / Divergent functions of the myotubularin (MTM) homologs AtMTM1 and AtMTM2 in Arabidopsis thaliana : Evolution of the plant MTM family. In: Plant Journal. 2012 ; Vol. 70, No. 5. pp. 866-878.
@article{32338a841d2c459986c7223d52583eeb,
title = "Divergent functions of the myotubularin (MTM) homologs AtMTM1 and AtMTM2 in Arabidopsis thaliana: Evolution of the plant MTM family",
abstract = "Myotubularin and myotubularin-related proteins are evolutionarily conserved in eukaryotes. Defects in their function result in muscular dystrophy, neuronal diseases and leukemia in humans. In contrast to the animal lineage, where genes encoding both active and inactive myotubularins (phosphoinositide 3-phosphatases) have appeared and proliferated in the basal metazoan group, myotubularin genes are not found in the unicellular relatives of green plants. However, they are present in land plants encoding proteins highly similar to the active metazoan enzymes. Despite their remarkable structural conservation, plant and animal myotubularins have significantly diverged in their functions. While loss of myotubularin function causes severe disease phenotypes in humans it is not essential for the cellular homeostasis under normal conditions in Arabidopsis thaliana. Instead, myotubularin deficiency is associated with altered tolerance to dehydration stress. The two Arabidopsis genes AtMTM1 and AtMTM2 have originated from a segmental chromosomal duplication and encode catalytically active enzymes. However, only AtMTM1 is involved in elevating the cellular level of phosphatidylinositol 5-phosphate in response to dehydration stress, and the two myotubularins differentially affect the Arabidopsis dehydration stress-responding transcriptome. AtMTM1 and AtMTM2 display different localization patterns in the cell, consistent with the idea that they associate with different membranes to perform specific functions. A single amino acid mutation in AtMTM2 (L250W) results in a dramatic loss of subcellular localization. Mutations in this region are linked to disease conditions in humans.",
keywords = "Arabidopsis MTM1, MTM2, evolution, plant myotubularins",
author = "Yong Ding and Ivan Ndamukong and Yang Zhao and Yuannan Xia and Riethoven, {Jean Jack} and Jones, {David R.} and Nullin Divecha and Zoya Avramova",
year = "2012",
month = "6",
day = "1",
doi = "10.1111/j.1365-313X.2012.04936.x",
language = "English (US)",
volume = "70",
pages = "866--878",
journal = "Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell",
number = "5",

}

TY - JOUR

T1 - Divergent functions of the myotubularin (MTM) homologs AtMTM1 and AtMTM2 in Arabidopsis thaliana

T2 - Evolution of the plant MTM family

AU - Ding, Yong

AU - Ndamukong, Ivan

AU - Zhao, Yang

AU - Xia, Yuannan

AU - Riethoven, Jean Jack

AU - Jones, David R.

AU - Divecha, Nullin

AU - Avramova, Zoya

PY - 2012/6/1

Y1 - 2012/6/1

N2 - Myotubularin and myotubularin-related proteins are evolutionarily conserved in eukaryotes. Defects in their function result in muscular dystrophy, neuronal diseases and leukemia in humans. In contrast to the animal lineage, where genes encoding both active and inactive myotubularins (phosphoinositide 3-phosphatases) have appeared and proliferated in the basal metazoan group, myotubularin genes are not found in the unicellular relatives of green plants. However, they are present in land plants encoding proteins highly similar to the active metazoan enzymes. Despite their remarkable structural conservation, plant and animal myotubularins have significantly diverged in their functions. While loss of myotubularin function causes severe disease phenotypes in humans it is not essential for the cellular homeostasis under normal conditions in Arabidopsis thaliana. Instead, myotubularin deficiency is associated with altered tolerance to dehydration stress. The two Arabidopsis genes AtMTM1 and AtMTM2 have originated from a segmental chromosomal duplication and encode catalytically active enzymes. However, only AtMTM1 is involved in elevating the cellular level of phosphatidylinositol 5-phosphate in response to dehydration stress, and the two myotubularins differentially affect the Arabidopsis dehydration stress-responding transcriptome. AtMTM1 and AtMTM2 display different localization patterns in the cell, consistent with the idea that they associate with different membranes to perform specific functions. A single amino acid mutation in AtMTM2 (L250W) results in a dramatic loss of subcellular localization. Mutations in this region are linked to disease conditions in humans.

AB - Myotubularin and myotubularin-related proteins are evolutionarily conserved in eukaryotes. Defects in their function result in muscular dystrophy, neuronal diseases and leukemia in humans. In contrast to the animal lineage, where genes encoding both active and inactive myotubularins (phosphoinositide 3-phosphatases) have appeared and proliferated in the basal metazoan group, myotubularin genes are not found in the unicellular relatives of green plants. However, they are present in land plants encoding proteins highly similar to the active metazoan enzymes. Despite their remarkable structural conservation, plant and animal myotubularins have significantly diverged in their functions. While loss of myotubularin function causes severe disease phenotypes in humans it is not essential for the cellular homeostasis under normal conditions in Arabidopsis thaliana. Instead, myotubularin deficiency is associated with altered tolerance to dehydration stress. The two Arabidopsis genes AtMTM1 and AtMTM2 have originated from a segmental chromosomal duplication and encode catalytically active enzymes. However, only AtMTM1 is involved in elevating the cellular level of phosphatidylinositol 5-phosphate in response to dehydration stress, and the two myotubularins differentially affect the Arabidopsis dehydration stress-responding transcriptome. AtMTM1 and AtMTM2 display different localization patterns in the cell, consistent with the idea that they associate with different membranes to perform specific functions. A single amino acid mutation in AtMTM2 (L250W) results in a dramatic loss of subcellular localization. Mutations in this region are linked to disease conditions in humans.

KW - Arabidopsis MTM1

KW - MTM2

KW - evolution

KW - plant myotubularins

UR - http://www.scopus.com/inward/record.url?scp=84861530795&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84861530795&partnerID=8YFLogxK

U2 - 10.1111/j.1365-313X.2012.04936.x

DO - 10.1111/j.1365-313X.2012.04936.x

M3 - Article

C2 - 22324391

AN - SCOPUS:84861530795

VL - 70

SP - 866

EP - 878

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 5

ER -