Home LiteratureArticle Details
PMID: 27327960 Published · epublish English Comparative Study Journal Article

Genome-Wide Characterization of Major Intrinsic Proteins in Four Grass Plants and Their Non-Aqua Transport Selectivity Profiles with Comparative Perspective.

PloS one ·Vol. 11 ·No. 6 ·2016-00-00 ·Pages e0157735

Azad AK, Ahmed J, Alum MA, Hasan MM, Ishikawa T, Sawa Y, Katsuhara M

Abstract

Major intrinsic proteins (MIPs), commonly known as aquaporins, transport not only water in plants but also other substrates of physiological significance and heavy metals. In most of the higher plants, MIPs are divided into five subfamilies (PIPs, TIPs, NIPs, SIPs and XIPs). Herein, we identified 68, 42, 38 and 28 full-length MIPs, respectively in the genomes of four monocot grass plants, specifically Panicum virgatum, Setaria italica, Sorghum bicolor and Brachypodium distachyon. Phylogenetic analysis showed that the grass plants had only four MIP subfamilies including PIPs, TIPs, NIPs and SIPs without XIPs. Based on structural analysis of the homology models and comparing the primary selectivity-related motifs [two NPA regions, aromatic/arginine (ar/R) selectivity filter and Froger's positions (FPs)] of all plant MIPs that have been experimentally proven to transport non-aqua substrates, we predicted the transport profiles of all MIPs in the four grass plants and also in eight other plants. Groups of MIP subfamilies based on ar/R selectivity filter and FPs were linked to the non-aqua transport profiles. We further deciphered the substrate selectivity profiles of the MIPs in the four grass plants and compared them with their counterparts in rice, maize, soybean, poplar, cotton, Arabidopsis thaliana, Physcomitrella patens and Selaginella moellendorffii. In addition to two NPA regions, ar/R filter and FPs, certain residues, especially in loops B and C, contribute to the functional distinctiveness of MIP groups. Expression analysis of transcripts in different organs indicated that non-aqua transport was related to expression of MIPs since most of the unexpressed MIPs were not predicted to facilitate the transport of non-aqua molecules. Among all MIPs in every plant, TIP (BdTIP1;1, SiTIP1;2, SbTIP2;1 and PvTIP1;2) had the overall highest mean expression. Our study generates significant information for understanding the diversity, evolution, non-aqua transport profiles and insight into comparative transport selectivity of plant MIPs, and provides tools for the development of transgenic plants.

MeSH Terms
Amino Acid Motifs Aquaporins/chemistry,genetics,metabolism Evolution, Molecular Gene Expression Regulation, Plant Genes, Plant Genome, Plant Plant Leaves/genetics Plant Proteins/chemistry,genetics,metabolism Plant Roots/genetics Plant Shoots/genetics Poaceae/genetics,metabolism Protein Transport Subcellular Fractions/metabolism Substrate Specificity Terminology as Topic Water/metabolism
Chemicals
Aquaporins Plant Proteins major intrinsic protein, plant Water
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Azad Abul Kalam
Department of Genetic Engineering and Biotechnology, Shahjalal University of Science and Technology, Sylhet 3114, Bangladesh.
Ahmed Jahed
Department of Genetic Engineering and Biotechnology, Shahjalal University of Science and Technology, Sylhet 3114, Bangladesh.
Alum Md Asraful
Forensic DNA Laboratory of Bangladesh Police, Malibagh, Dhaka, Bangladesh.
Hasan Md Mahbub
Department of Genetic Engineering and Biotechnology, University of Chittagong, Chittagong 4331, Bangladesh.
Ishikawa Takahiro
Department of Life Science and Biotechnology, Shimane University, Shimane 690-8504, Japan.
Sawa Yoshihiro
Department of Life Science and Biotechnology, Shimane University, Shimane 690-8504, Japan.
Katsuhara Maki
Institute of Plant Science and Resources, Okayama University, Chuo-2-chome, Kurashiki 710-0046, Japan.
References (69)
69 references, click to expand
  1. Structural clues in the sequences of the aquaporins.
    J Mol Biol. 2000 Jan 28;295(4):1039-53 PMID: 10656809
  2. Structure of a glycerol-conducting channel and the basis for its selectivity.
    Science. 2000 Oct 20;290(5491):481-6 PMID: 11039922
  3. Aquaporins constitute a large and highly divergent protein family in maize.
    Plant Physiol. 2001 Mar;125(3):1206-15 PMID: 11244102
  4. The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants.
    Plant Physiol. 2001 Aug;126(4):1358-69 PMID: 11500536
  5. Structural basis of water-specific transport through the AQP1 water channel.
    Nature. 2001 Dec 20-27;414(6866):872-8 PMID: 11780053
  6. A new subfamily of major intrinsic proteins in plants.
    Mol Biol Evol. 2002 Apr;19(4):456-61 PMID: 11919287
  7. Control of the selectivity of the aquaporin water channel family by global orientational tuning.
    Science. 2002 Apr 19;296(5567):525-30 PMID: 11964478
  8. Interactions between plasma membrane aquaporins modulate their water channel activity.
    Plant Cell. 2004 Jan;16(1):215-28 PMID: 14671024
  9. Phosphorylation of plasma membrane aquaporin regulates temperature-dependent opening of tulip petals.
    Plant Cell Physiol. 2004 May;45(5):608-17 PMID: 15169943
  10. Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter.
    Plant Physiol. 2004 Jun;135(2):1059-68 PMID: 15181215
  11. Aquaporin homologues in plants and mammals transport ammonia.
    FEBS Lett. 2004 Sep 10;574(1-3):31-6 PMID: 15358535
  12. Phylogeny and evolution of the major intrinsic protein family.
    Biol Cell. 2005 Jun;97(6):397-414 PMID: 15850454
  13. Identification of 33 rice aquaporin genes and analysis of their expression and function.
    Plant Cell Physiol. 2005 Sep;46(9):1568-77 PMID: 16033806
  14. Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana.
    FEBS Lett. 2005 Oct 24;579(25):5814-20 PMID: 16223486
  15. Gene identification in novel eukaryotic genomes by self-training algorithm.
    Nucleic Acids Res. 2005 Nov 28;33(20):6494-506 PMID: 16314312
  16. Structural mechanism of plant aquaporin gating.
    Nature. 2006 Feb 9;439(7077):688-94 PMID: 16340961
  17. Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels.
    Biochemistry. 2005 Dec 27;44(51):16826-34 PMID: 16363796
  18. Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons.
    Proc Natl Acad Sci U S A. 2006 Jan 10;103(2):269-74 PMID: 16407156
  19. Aquaporin subfamily with unusual NPA boxes.
    Biochim Biophys Acta. 2006 Aug;1758(8):989-93 PMID: 16579962
  20. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation.
    Plant Cell. 2006 Jun;18(6):1498-509 PMID: 16679457
  21. The billion-ton biofuels vision.
    Science. 2006 Jun 2;312(5778):1277 PMID: 16741078
  22. Silicon uptake and accumulation in higher plants.
    Trends Plant Sci. 2006 Aug;11(8):392-7 PMID: 16839801
  23. Aquaporins: a promising target for drug development.
    Expert Opin Ther Targets. 2006 Dec;10(6):889-909 PMID: 17105375
  24. Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants.
    Planta. 2007 Aug;226(3):729-40 PMID: 17443343
  25. Homology modeling of major intrinsic proteins in rice, maize and Arabidopsis: comparative analysis of transmembrane helix association and aromatic/arginine selectivity filters.
    BMC Struct Biol. 2007 Apr 19;7:27 PMID: 17445256
  26. Aquaporins and plant leaf movements.
    Ann Bot. 2008 Jan;101(1):1-4 PMID: 18024416
  27. A molecular modeling approach defines a new group of Nodulin 26-like aquaporins in plants.
    Biochem Biophys Res Commun. 2008 Feb 29;367(1):60-6 PMID: 18155659
  28. Characterization of substrate specificity of a rice silicon transporter, Lsi1.
    Pflugers Arch. 2008 Jul;456(4):679-86 PMID: 18214526
  29. Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability.
    Plant Cell. 2008 Mar;20(3):648-57 PMID: 18349152
  30. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens.
    BMC Plant Biol. 2008 Apr 22;8:45 PMID: 18430224
  31. Plant aquaporins: membrane channels with multiple integrated functions.
    Annu Rev Plant Biol. 2008;59:595-624 PMID: 18444909
  32. Plant plasma membrane water channels conduct the signalling molecule H2O2.
    Biochem J. 2008 Aug 15;414(1):53-61 PMID: 18462192
  33. A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes.
    BMC Biol. 2008 Jun 10;6:26 PMID: 18544156
  34. Characterization of four plasma membrane aquaporins in tulip petals: a putative homolog is regulated by phosphorylation.
    Plant Cell Physiol. 2008 Aug;49(8):1196-208 PMID: 18567892
  35. NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis.
    Plant Cell. 2008 Oct;20(10):2860-75 PMID: 18952773
  36. AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea.
    FEBS Lett. 2008 Dec 10;582(29):4077-82 PMID: 19022253
  37. The Sorghum bicolor genome and the diversification of grasses.
    Nature. 2009 Jan 29;457(7229):551-6 PMID: 19189423
  38. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms.
    Biochim Biophys Acta. 2009 Jun;1788(6):1213-28 PMID: 19327343
  39. PoreWalker: a novel tool for the identification and characterization of channels in transmembrane proteins from their three-dimensional structure.
    PLoS Comput Biol. 2009 Jul;5(7):e1000440 PMID: 19609355
  40. A look inside: localization patterns and functions of intracellular plant aquaporins.
    New Phytol. 2009 Oct;184(2):289-302 PMID: 19674338
  41. 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 PMID: 19930558
  42. Genome sequencing and analysis of the model grass Brachypodium distachyon.
    Nature. 2010 Feb 11;463(7282):763-8 PMID: 20148030
  43. Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis.
    Plant Cell Physiol. 2010 May;51(5):767-75 PMID: 20360019
  44. On the evolutionary conservation of hydrogen bonds made by buried polar amino acids: the hidden joists, braces and trusses of protein architecture.
    BMC Evol Biol. 2010 May 31;10:161 PMID: 20513243
  45. Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.).
    BMC Plant Biol. 2010 Jul 13;10:142 PMID: 20626869
  46. Mapping of tonoplast intrinsic proteins in maturing and germinating Arabidopsis seeds reveals dual localization of embryonic TIPs to the tonoplast and plasma membrane.
    Mol Plant. 2011 Jan;4(1):180-9 PMID: 20833734
  47. TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana.
    Plant J. 2010 Dec;64(6):1038-47 PMID: 21143683
  48. Vacuolar proton pumps and aquaporins involved in rapid internode elongation of deepwater rice.
    Biosci Biotechnol Biochem. 2011;75(1):114-22 PMID: 21228479
  49. Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates.
    Plant J. 2011 Apr;66(2):306-17 PMID: 21241387
  50. Plant aquaporins with non-aqua functions: deciphering the signature sequences.
    Plant Mol Biol. 2011 Mar;75(4-5):413-30 PMID: 21308399
  51. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
    Mol Biol Evol. 2011 Oct;28(10):2731-9 PMID: 21546353
  52. The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO₂ transport facilitator.
    Plant J. 2011 Sep;67(5):795-804 PMID: 21564354
  53. Chloroplast genome variation in upland and lowland switchgrass.
    PLoS One. 2011;6(8):e23980 PMID: 21887356
  54. Substitution of a single amino acid residue in the aromatic/arginine selectivity filter alters the transport profiles of tonoplast aquaporin homologs.
    Biochim Biophys Acta. 2012 Jan;1818(1):1-11 PMID: 21963407
  55. Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants.
    Transgenic Res. 2012 Dec;21(6):1265-77 PMID: 22350764
  56. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential.
    Nat Biotechnol. 2012 May 13;30(6):549-54 PMID: 22580950
  57. Annotation of Selaginella moellendorffii Major Intrinsic Proteins and the Evolution of the Protein Family in Terrestrial Plants.
    Front Plant Sci. 2012 Feb 20;3:33 PMID: 22639644
  58. Expression profiles of aquaporin homologues and petal movement during petal development in Tulipa gesneriana.
    Physiol Plant. 2013 Jul;148(3):397-407 PMID: 23088645
  59. Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.).
    PLoS One. 2013;8(2):e56312 PMID: 23437113
  60. Loop A is critical for the functional interaction of two Beta vulgaris PIP aquaporins.
    PLoS One. 2013;8(3):e57993 PMID: 23483963
  61. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide.
    Biochim Biophys Acta. 2014 May;1840(5):1596-604 PMID: 24060746
  62. Genome-wide analysis and expression profiling of the Solanum tuberosum aquaporins.
    Plant Physiol Biochem. 2013 Dec;73:392-404 PMID: 24215931
  63. Genome-wide identification and expression analysis of aquaporins in tomato.
    PLoS One. 2013 Nov 19;8(11):e79052 PMID: 24260152
  64. Aquaglyceroporins: generalized metalloid channels.
    Biochim Biophys Acta. 2014 May;1840(5):1583-91 PMID: 24291688
  65. Prediction of aquaporin function by integrating evolutionary and functional analyses.
    J Membr Biol. 2014 Feb;247(2):107-25 PMID: 24292667
  66. Heteromerization of PIP aquaporins affects their intrinsic permeability.
    Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):231-6 PMID: 24367080
  67. CO2 transport by PIP2 aquaporins of barley.
    Plant Cell Physiol. 2014 Feb;55(2):251-7 PMID: 24406630
  68. High and Low Affinity Urea Root Uptake: Involvement of NIP5;1.
    Plant Cell Physiol. 2015 Aug;56(8):1588-97 PMID: 25957355
  69. Prediction of functional residues in water channels and related proteins.
    Protein Sci. 1998 Jun;7(6):1458-68 PMID: 9655351
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2016-00-00
Epub
2016-00-21
Pages
e0157735
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC4915720
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com