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

• Published in: The Plant journal : for cell and molecular biology Vol. 70; no. 5; pp. 866 - 878
• Main Authors: Ding, Yong, Ndamukong, Ivan, Zhao, Yang, Xia, Yuannan, Riethoven, Jean‐Jack, Jones, David R., Divecha, Nullin, Avramova, Zoya
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01.06.2012; Blackwell
• Subjects: Amino Acid Substitution; Amino acids; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis MTM1; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Biological and medical sciences; Chromosome Duplication; Chromosomes, Plant - genetics; Chromosomes, Plant - metabolism; Dehydration - metabolism; Enzyme Activation; Eukaryotes; evolution; Evolution, Molecular; Evolutionary biology; Fundamental and applied biological sciences. Psychology; Gene expression; Gene Expression Regulation, Plant; Genes, Plant; Mitochondrial Proteins - genetics; Mitochondrial Proteins - metabolism; MTM2; Mutation; Oligonucleotide Array Sequence Analysis - methods; Phosphatidylinositol Phosphates - metabolism; Phosphoric Monoester Hydrolases - genetics; Phosphoric Monoester Hydrolases - metabolism; Plant biology; Plant Cells - metabolism; plant myotubularins; Plant physiology and development; Plants, Genetically Modified - genetics; Plants, Genetically Modified - metabolism; Protein Structure, Tertiary; Protein Tyrosine Phosphatases, Non-Receptor - genetics; Protein Tyrosine Phosphatases, Non-Receptor - metabolism; Proteins; Recombinant Fusion Proteins - genetics; Recombinant Fusion Proteins - metabolism; Soil; Stress, Physiological; Transcriptome; Arabidopsis thaliana; Molecular evolution; plant myotubularins; Plant; Vegetals; Cruciferae; Dicotyledones; Angiospermae; MTM2; Arabidopsis MTM1; Spermatophyta; evolution
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/j.1365-313X.2012.04936.x

Summary 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.