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Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective.
BMC Plant Biol. 2009 Nov 20; 9:134.BP

Abstract

BACKGROUND

Members of major intrinsic proteins (MIPs) include water-conducting aquaporins and glycerol-transporting aquaglyceroporins. MIPs play important role in plant-water relations. The model plants Arabidopsis thaliana, rice and maize contain more than 30 MIPs and based on phylogenetic analysis they can be divided into at least four subfamilies. Populus trichocarpa is a model tree species and provides an opportunity to investigate several tree-specific traits. In this study, we have investigated Populus MIPs (PtMIPs) and compared them with their counterparts in Arabidopsis, rice and maize.

RESULTS

Fifty five full-length MIPs have been identified in Populus genome. Phylogenetic analysis reveals that Populus has a fifth uncharacterized subfamily (XIPs). Three-dimensional models of all 55 PtMIPs were constructed using homology modeling technique. Aromatic/arginine (ar/R) selectivity filters, characteristics of loops responsible for solute selectivity (loop C) and gating (loop D) and group conservation of small and weakly polar interfacial residues have been analyzed. Majority of the non-XIP PtMIPs are similar to those in Arabidopsis, rice and maize. Additional XIPs were identified from database search and 35 XIP sequences from dicots, fungi, moss and protozoa were analyzed. Ar/R selectivity filters of dicots XIPs are more hydrophobic compared to fungi and moss XIPs and hence they are likely to transport hydrophobic solutes. Loop C is longer in one of the subgroups of dicot XIPs and most probably has a significant role in solute selectivity. Loop D in dicot XIPs has higher number of basic residues. Intron loss is observed on two occasions: once between two subfamilies of eudicots and monocot and in the second instance, when dicot and moss XIPs diverged from fungi. Expression analysis of Populus MIPs indicates that Populus XIPs don't show any tissue-specific transcript abundance.

CONCLUSION

Due to whole genome duplication, Populus has the largest number of MIPs identified in any single species. Non-XIP MIPs are similar in all four plant species considered in this study. Small and weakly polar residues at the helix-helix interface are group conserved presumably to maintain the hourglass fold of MIP channels. Substitutions in ar/R selectivity filter, insertion/deletion in loop C, increasing basic nature of loop D and loss of introns are some of the events occurred during the evolution of dicot XIPs.

Authors+Show Affiliations

Department of Biological Sciences and Bioengineering, Indian Institute of Technology Kanpur, Kanpur 208016, India. anjalib@iitk.ac.inNo affiliation info available

Pub Type(s)

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

Language

eng

PubMed ID

19930558

Citation

Gupta, Anjali Bansal, and Ramasubbu Sankararamakrishnan. "Genome-wide Analysis of Major Intrinsic Proteins in the Tree Plant Populus Trichocarpa: Characterization of XIP Subfamily of Aquaporins From Evolutionary Perspective." BMC Plant Biology, vol. 9, 2009, p. 134.
Gupta AB, Sankararamakrishnan R. Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol. 2009;9:134.
Gupta, A. B., & Sankararamakrishnan, R. (2009). Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biology, 9, 134. https://doi.org/10.1186/1471-2229-9-134
Gupta AB, Sankararamakrishnan R. Genome-wide Analysis of Major Intrinsic Proteins in the Tree Plant Populus Trichocarpa: Characterization of XIP Subfamily of Aquaporins From Evolutionary Perspective. BMC Plant Biol. 2009 Nov 20;9:134. PubMed PMID: 19930558.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. AU - Gupta,Anjali Bansal, AU - Sankararamakrishnan,Ramasubbu, Y1 - 2009/11/20/ PY - 2008/09/03/received PY - 2009/11/20/accepted PY - 2009/11/26/entrez PY - 2009/11/26/pubmed PY - 2010/1/28/medline SP - 134 EP - 134 JF - BMC plant biology JO - BMC Plant Biol VL - 9 N2 - BACKGROUND: Members of major intrinsic proteins (MIPs) include water-conducting aquaporins and glycerol-transporting aquaglyceroporins. MIPs play important role in plant-water relations. The model plants Arabidopsis thaliana, rice and maize contain more than 30 MIPs and based on phylogenetic analysis they can be divided into at least four subfamilies. Populus trichocarpa is a model tree species and provides an opportunity to investigate several tree-specific traits. In this study, we have investigated Populus MIPs (PtMIPs) and compared them with their counterparts in Arabidopsis, rice and maize. RESULTS: Fifty five full-length MIPs have been identified in Populus genome. Phylogenetic analysis reveals that Populus has a fifth uncharacterized subfamily (XIPs). Three-dimensional models of all 55 PtMIPs were constructed using homology modeling technique. Aromatic/arginine (ar/R) selectivity filters, characteristics of loops responsible for solute selectivity (loop C) and gating (loop D) and group conservation of small and weakly polar interfacial residues have been analyzed. Majority of the non-XIP PtMIPs are similar to those in Arabidopsis, rice and maize. Additional XIPs were identified from database search and 35 XIP sequences from dicots, fungi, moss and protozoa were analyzed. Ar/R selectivity filters of dicots XIPs are more hydrophobic compared to fungi and moss XIPs and hence they are likely to transport hydrophobic solutes. Loop C is longer in one of the subgroups of dicot XIPs and most probably has a significant role in solute selectivity. Loop D in dicot XIPs has higher number of basic residues. Intron loss is observed on two occasions: once between two subfamilies of eudicots and monocot and in the second instance, when dicot and moss XIPs diverged from fungi. Expression analysis of Populus MIPs indicates that Populus XIPs don't show any tissue-specific transcript abundance. CONCLUSION: Due to whole genome duplication, Populus has the largest number of MIPs identified in any single species. Non-XIP MIPs are similar in all four plant species considered in this study. Small and weakly polar residues at the helix-helix interface are group conserved presumably to maintain the hourglass fold of MIP channels. Substitutions in ar/R selectivity filter, insertion/deletion in loop C, increasing basic nature of loop D and loss of introns are some of the events occurred during the evolution of dicot XIPs. SN - 1471-2229 UR - https://www.unboundmedicine.com/medline/citation/19930558/Genome_wide_analysis_of_major_intrinsic_proteins_in_the_tree_plant_Populus_trichocarpa:_characterization_of_XIP_subfamily_of_aquaporins_from_evolutionary_perspective_ L2 - https://bmcplantbiol.biomedcentral.com/articles/10.1186/1471-2229-9-134 DB - PRIME DP - Unbound Medicine ER -