Plant Molecular Biology

, Volume 91, Issue 4–5, pp 375–396 | Cite as

The Hevea brasiliensis XIP aquaporin subfamily: genomic, structural and functional characterizations with relevance to intensive latex harvesting

  • David Lopez
  • Maroua Ben Amira
  • Daniel Brown
  • Beatriz Muries
  • Nicole Brunel-Michac
  • Sylvain Bourgerie
  • Benoit Porcheron
  • Remi Lemoine
  • Hervé Chrestin
  • Ewan Mollison
  • Alessandra Di Cola
  • Lorenzo Frigerio
  • Jean-Louis Julien
  • Aurélie Gousset-Dupont
  • Boris Fumanal
  • Philippe Label
  • Valérie Pujade-Renaud
  • Daniel AuguinEmail author
  • Jean-Stéphane VenisseEmail author


X-Intrinsic Proteins (XIP) were recently identified in a narrow range of plants as a full clade within the aquaporins. These channels reportedly facilitate the transport of a wide range of hydrophobic solutes. The functional roles of XIP in planta remain poorly identified. In this study, we found three XIP genes (HbXIP1;1, HbXIP2;1 and HbXIP3;1) in the Hevea brasiliensis genome. Comprehensive bioinformatics, biochemical and structural analyses were used to acquire a better understanding of this AQP subfamily. Phylogenetic analysis revealed that HbXIPs clustered into two major groups, each distributed in a specific lineage of the order Malpighiales. Tissue-specific expression profiles showed that only HbXIP2;1 was expressed in all the vegetative tissues tested (leaves, stem, bark, xylem and latex), suggesting that HbXIP2;1 could take part in a wide range of cellular processes. This is particularly relevant to the rubber-producing laticiferous system, where this isoform was found to be up-regulated during tapping and ethylene treatments. Furthermore, the XIP transcriptional pattern is significantly correlated to latex production level. Structural comparison with SoPIP2;1 from Spinacia oleracea species provides new insights into the possible role of structural checkpoints by which HbXIP2;1 ensures glycerol transfer across the membrane. From these results, we discuss the physiological involvement of glycerol and HbXIP2;1 in water homeostasis and carbon stream of challenged laticifers. The characterization of HbXIP2;1 during rubber tree tapping lends new insights into molecular and physiological response processes of laticifer metabolism in the context of latex exploitation.


XIP aquaporin Hevea brasiliensis Latex Evolution Glycerol Cell homeostasis 



We are in Professor François Chaumont’s debt for reading carefully the manuscript and for his constructive remarks that helped us to improve it with relevant arguments. We thank Sylvaine Blateyron for her excellent technical support. This research was supported by the earmarked funds from the PIAF and LBLGC Research Systems. The funders -whatever this may mean- had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We would also like to thank the anonymous reviewers for their constructive comments and encouragement on the article. The authors declare no competing financial interests.

Author Contributions

David Lopez co-designed and participated to most of the experiments and wrote the first draft of the article; Jean-Stéphane Venisse, Beatriz Muries and Maroua Ben Amira carried out the gene expression experiments and bioinformatics analysis; Nicole Brunel-Michac carried out and interpreted the in situ hybridization experiments; Daniel Auguin performed the HbXIP2;1 3D structure modeling and the structural analysis; Sylvain Bourgerie performed water permeability assessment in yeast and the functional complementation of Dfps1 yeast strain; Benoit Porcheron and Rémy Lemoine preformed glycerol permeability; Daniel Brown and Lorenzo Frigerio directed and performed YFP-HbXIP2;1 construction, agro-infiltration of tobacco and confocal microscopy analysis, and appropriate interpretation; Ewan Mollison and Alessandra Di Cola retrieved full-length HbXIP sequences in H. brasiliensis genome; Hervé Chrestin provided the latex yield data; Jean-Stéphane Venisse and Boris Fumanal performed and interpreted the phylogenetic analysis; Aurélie Gousset-Dupont, Philippe Label, Valérie Pujade-Renaud and Jean-Louis Julien have ensured a critical examination of the manuscript; Valérie Pujade-Renaud provided plant materials needed for this work; Jean-Stéphane Venisse led the program, co-designed the experiments, obtained the funding, and coordinated and compiled authors’ contributions to the final version of the article; Daniel Auguin and Jean-Stéphane Venisse wrote the final draft of the article and edited it; All the authors participated in the analysis of data, and collectively approved whole of the result interpretation and related hypothesis.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11103_2016_462_MOESM1_ESM.docx (160 kb)
Supplementary Fig. S1 XIP nucleic and protein sequences of HbXIP1;1, HbXIP2;1 and HbXIP3;1 isoforms from H. brasiliensis (DOCX 160 kb)
11103_2016_462_MOESM2_ESM.pdf (30 kb)
Supplementary Fig. S2 Amino acid identity and similarity percentages between H. brasiliensis XIP protein sequences and the three phylogenic XIP clusters (identity/similarity). Percentages were calculated using the BLAST algorithm. Theoretical prediction of the biochemical properties of HbXIP (amino acids number, AA ; calculated protein molecular weight, MW g.mol-1; theoretical protein isoelectric point, pI) (PDF 30 kb)
11103_2016_462_MOESM3_ESM.pdf (31.7 mb)
Supplementary Fig. S3 Multiple sequence alignment annotated on the basis of a structural alignment. a Restricted Multiple Sequence Alignment of MIP (PIP and XIP) from the plant kingdom using the MUSCLE routine embedded in Jalview and further enriched by the clustalX scheme. H. brasiliensis HbXIPs are confronted with both plant XIP from Clusters II and IV (Fig 1a), and three PIP (SoPIP2;1, HbPIP1;1 and HbPIP2;2). SoPIP2;1 was chosen to delineate the conserved topological elements along the sequence progression. Sequences were ordered according to their average proximity using a BLOSUM62 substitution matrix (distance tree). Arrows on the left of the sequence names point out the chosen candidates for a structure and function comparison based on modeling within this study. Concerning the two latter, the amino acids delineating the channel lumen have their sequence positions indicated by a blue circle under the alignment. AQP canonical signatures are named according to the literature above the topological scheme. By analogy with the structure of SoPIP2;1, for which the position of the cystine is recalled, a plausible intermolecular disulfide bridge is proposed at the carboxy-terminal anchor of the LD loop as an active element in the cooperative functioning of the common AQP native tetrameric assembly of HbXIP2;1. b Trace representation of the superimposition performed by Mustang in order to compare, at the amino acids scale, the composition of the pores between the I-TASSER model of HbXIP2;1 with the high resolution structure of SoPIP2;1. HbXIP2;1 is shown in green SoPIP2;1 in magenta. The 3D alignment has a score of 34.13% of sequence identity and the superimposition root-mean-square deviation (RMSD) is given at 1.01Å over 208 aligned residues. c Crossed-eyed stereo view of the relative orientations of the similar residues and backbone carbonyls in the lumen of both channels (PDF 32466 kb)
11103_2016_462_MOESM4_ESM.pdf (1.4 mb)
Supplementary Fig. S4 Homology modeling result of the tetrameric HbXIP2;1 from H. brasiliensis rebuilt using the tetrameric spinach aquaporin SoPIP2;1 as a template on which a model out of I-TASSER was superimposed and further minimized with CHARMM-GUI. a Ribbon diagram of the quaternary protein complex showing the four subunits (green, yellow, orange, blue). The glycerol molecule, shown in spacefill balls, is placed by I-TASSER in the cytoplasmic vestibule. The sidechains and backbone carbonyls making up the interface of the lumen of the pore are shown in sticks. The putative cystine where a cooperativity for the concerted opening of the two gates could take place is presented in the inner side. b Zoom (from the cytosolic compartment) on the glycerol entering the channel (PDF 1413 kb)
11103_2016_462_MOESM5_ESM.pdf (1.9 mb)
Supplementary Fig. S5 Froger’s residues and their relative position on the modelled structure of HbXIP2;1. Focus on the five positions (mauve): the sidechains of the so-called Froger’s amino acids appear relatively distant from the central channel (orange grid) of one subunit (green cartoons), suggesting more a structural role than a selectivity role for these (PDF 1957 kb)
11103_2016_462_MOESM6_ESM.pdf (84 kb)
Supplementary Fig. S6 Detailed presentation of Fig. 6b including statistical analysis of the constitutive transcript accumulation of the expressed HbPIP1s (a), HbPIP2s (b) and HbPLTs (c) genes in various vegetative organs from H. brasiliensis (clone PB217). Leaf samples 1, 2, and 3 are young, adult and senescent leaves, respectively. Branch samples 1, 2, 3 and 4 are growing apical parts of stem, bark, wood and latex, respectively. Expression was monitored using real-time quantitative RT-PCR analyses and normalized with the expression of three housekeeping genes (HbACT, HbCYP and Hb18S rRNA). Arbitrary unit calculation is detailed in Materials and Methods. Data correspond to means of three technical repeats from three independent biological experiments, and bars represent the biological standard deviation (PDF 83 kb)
11103_2016_462_MOESM7_ESM.pdf (515 kb)
Supplementary Fig. S7 Stem transverse section (10 µm thick) stained with toluidine blue to identify the cell structures. Scale bar indicates 50 μm (PDF 515 kb)
11103_2016_462_MOESM8_ESM.pdf (998 kb)
Supplementary Fig. S8 a Original photographs in which consensus selected zones (red squares) were joined up to create the artificial pictures ABC of the Fig 7. b Alkaline phosphatase staining controls without probe. Scale bar indicates 50 μm (PDF 998 kb)
11103_2016_462_MOESM9_ESM.pdf (136 kb)
Supplementary Fig.S9 Detailed presentation of Fig. 8b including statistical analysis of HbPIP1s (a), HbPIP2s (b) and HbPLTs (c) gene expression in latex and bark of exploited H. brasiliensis trees (clone PB217). Samples were collected on two successive tapping days (TAP1 and TAP2), from trees treated with ethylene respectively 4h, 8h, 16h, 24h and 40h before the first tapping. Expression was monitored using real-time quantitative RT-PCR and normalized by the expression of three housekeeping genes (HbACT, HbCYP and Hb18S rRNA). Relative expression rate was obtained following by E -ΔΔCt method, with the untreated samples as controls. Data correspond to means of three technical repeats from two independent biological experiments, and bars represent the biological standard deviation (PDF 136 kb)
11103_2016_462_MOESM10_ESM.pptx (10.9 mb)
Supplementary Fig. S10 High-definition format of Fig. 2 (PPTX 11205 kb)
11103_2016_462_MOESM11_ESM.xlsx (52 kb)
Supplementary Tab. S1 Features of the non-redundant representative Viridiplantae XIP proteins and two H. brasiliensis PIP proteins (HbPIP1;1 and HbPIP2;1) used in the phylogenetic analysis (XLSX 52 kb)
11103_2016_462_MOESM12_ESM.xlsx (13 kb)
Supplementary Tab. S2 Primers used for qPCR amplification, in situ hybridization, yeast experiments and ectopic expressions in tobacco (XLSX 13 kb)


  1. Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic protein. Biochim Biophys Acta 1840:1468–1481PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedPubMedCentralCrossRefGoogle Scholar
  3. An F, Zou Z, Cai X, Wang J, Rookes J, Lin W, Cahill D, Kong L (2015) Regulation of HbPIP2;3, a latex-abundant water transporter, is associated with latex dilution and yield in the rubber tree (Hevea brasiliensis Muell. Arg.). PLoS one 10:e0125595PubMedPubMedCentralCrossRefGoogle Scholar
  4. Anderberg HI, Danielson JAH, Johanson U (2011) Algal MIPs, high diversity and conserved motifs. BMC Evol Biol 11:110PubMedPubMedCentralCrossRefGoogle Scholar
  5. Anderberg HI, Kjellbom P, Johanson U (2012) Annotation of Selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants. Front Plant Sci 3:33PubMedPubMedCentralCrossRefGoogle Scholar
  6. Anderca MI, Suga S, Furuichi T, Shimogawara K, Maeshima M, Muto S (2004) Functional identification of the glycerol transport activity of Chlamydomonas reinhardtii CrMIP1. Plant Cell Physiol 45:1313–1319PubMedCrossRefGoogle Scholar
  7. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98:10037–10041PubMedPubMedCentralCrossRefGoogle Scholar
  8. Barlowe C (2003) Signals for COPII-dependent export from the ER: What’s the ticket out? Trends Cell Biol 13:295–300PubMedCrossRefGoogle Scholar
  9. Bienert GP, Bienert MD, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66:306–317PubMedCrossRefGoogle Scholar
  10. Bienert GP, Cavez D, Besserer A, Berny MC, Gilis D, Rooman M, Chaumont F (2012) A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomers. Biochem J 445:101–111PubMedCrossRefGoogle Scholar
  11. Brooks BR, Brooks CL, Mackerell AD, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, Caflisch A, Caves L, Cui Q, Dinner AR, Feig M, Fischer S, Gao J, Hodoscek M, Im W, Kuczera K, Lazaridis T, Ma J, Ovchinnikov V, Paci E, Pastor RW, Post CB, Pu JZ, Schaefer M, Tidor B, Venable RM, Woodcock HL, Wu X, Yang W, York DM, Karplus M (2009) CHARMM: the biomolecular simulation program. J Comput Chem 30:1545–1614PubMedPubMedCentralCrossRefGoogle Scholar
  12. Brunel N, Leduc N, Poupard P, Simoneau P, Mauget JC, Viemont JD (2002) KNAP2, a class I KN1-like gene is a negative marker of bud growth potential in apple tress (Malus domestica L. Borkh.). J Exp Bot 53:2143–2149PubMedCrossRefGoogle Scholar
  13. Chanda B, Venugopal SC, Kulshrestha S, Navarre D, Downie B, Vaillancourt L, Kachroo A, Kachroo P (2008) Glycerol-3-phosphate levels are associated with basal resistance to the hemibiotrophic fungus Colletotrichum higginsianum in Arabidopsis. Plant Physiol 147:2017–2029PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chao J, Chen Y, Wu S, Tian WM (2015) Comparative transcriptome analysis of latex from rubber tree clone CATAS8-79 and PR107 reveals new cues for the regulation of latex regeneration and duration of latex flow. BMC Plant Biol 15:104PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chase MW, Reveal JL (2009) A phylogenetic classification of the land plants to accompany APG III. Bot J Linn Soc 161:122–127CrossRefGoogle Scholar
  16. Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164:1600–1618PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764PubMedCrossRefGoogle Scholar
  18. Chen LY (2013) Glycerol modulates water permeation through Escherichia coli aquaglyceroporin GlpF. Biochim Biophys Acta 1828:1786–1793PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257PubMedCrossRefGoogle Scholar
  20. Chen VB, Arendall WB, Head JJ, Immornino RM, Kapral GL, Murray LW, Richardson JS, Richardson DC (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66:12–21PubMedCrossRefGoogle Scholar
  21. Chevenet F, Brun C, Banuls AL, Jacq B, Chisten R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7:439PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chothia C (1975) Structural invariants in protein folding. Nature 254:304–308PubMedCrossRefGoogle Scholar
  23. Chow KS, Wan KL, Isa MN, Bahari A, Tan SH, Harikrishna K, Yeang HY (2007) Insights into rubber biosynthesis from transcriptome analysis of Hevea brasiliensis latex. J Exp Bot 58:2429–2440PubMedCrossRefGoogle Scholar
  24. Chow KS, Isa MN, Bahari A, Ghazali AK, Alias H, Zainuddin Z, Hoh CC, Wan KL (2012) Metabolic routes affecting rubber biosynthesis in Hevea brasiliensis latex. J Exp Bot 63:1863–1871PubMedCrossRefGoogle Scholar
  25. Cornish K (2001) Similarities and differences in rubber biochemistry among plant species. Phytochemistry 57:1123–1134PubMedCrossRefGoogle Scholar
  26. Coupé M, Chrestin H (1989) Physico-chemical and bio-chemical mechanisms of the hormonal (ethylene) stimulation: early biochemical events induced in Hevea latex by hormonal bark stimulation. In: d’Auzac J, Jacob JL, Chrestin H (eds) Physiology of rubber tree latex. CRC Press Inc., Boca Raton, pp 295–319Google Scholar
  27. D’Auzac J, Ribaillier D (1969) Ethylene: a new stimulant of latex yield for Hevea brasiliensis. CR Acad Sci D Sci Nat 268:3046–3049Google Scholar
  28. D’Auzac J, Jacob JL, Prévôt JC, Clément A, Gallois R (1997) The regulation of cis-polyisoprene production (natural rubber) from Hevea brasiliensis. In: Pandalai SG (ed) Recent research developments in plant physiology. Research Singpost, Trivandrum, pp 273–332Google Scholar
  29. Danielson JAH, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8:45PubMedPubMedCentralCrossRefGoogle Scholar
  30. De Fay E, Sanier C, Hebant C (1989) Distribution of plasmodesmata in the phloem of Hevea brasiliensis in relation to laticifer loading. Protoplasma 149:155–162CrossRefGoogle Scholar
  31. DeLano WL (2004) PyMOL User’s Guide. DeLano Scientific, San Carlos, p 2004Google Scholar
  32. Di Giorgio JP, Soto G, Alleva K, Jozefkowicz C, Amodeo G, Muschietti JP, Ayub ND (2014) Prediction of aquaporin function by integrating evolutionary and functional analyses. J Membr Biol 247:107–125CrossRefGoogle Scholar
  33. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, Klebe G, Baker NA (2007) PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res 35:W522–W525PubMedPubMedCentralCrossRefGoogle Scholar
  34. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  35. Du H, Brender JR, Zhang J, Zhang Y (2015) Protein structure prediction provides comparable performance to crystallographic structures in docking-based virtual screening. Methods 71:77–84PubMedCrossRefGoogle Scholar
  36. Dusotoit-Coucaud A, Brunel N, Kongsawadworakul P, Viboonjun U, Lacointe A, Julien JL, Chrestin H, Sakr S (2009) Sucrose importation into laticifers of Hevea brasiliensis, in relation to ethylene stimulation of latex production. Ann Bot 104:635–647PubMedPubMedCentralCrossRefGoogle Scholar
  37. Dusotoit-Coucaud A, Kongsawadworakul P, Maurousset L, Viboonjun U, Brunel N, Pujade-Renaud V, Chrestin H, Sakr S (2010a) Ethylene stimulation of latex yield depends on the expression of a sucrose transporter (HbSUT1B) in rubber tree (Hevea brasiliensis). Tree Physiol 30:1586–1598PubMedCrossRefGoogle Scholar
  38. Dusotoit-Coucaud A, Porcheron B, Brunel N, Kongsawadworakul P, Franchel J, Viboonjun U, Chretin H, Lemoine R, Sakr S (2010b) Cloning and characterization of a new polyol transporter (HbPLT2) in Hevea brasiliensis. Plant Cell Physiol 51:1878–1888PubMedCrossRefGoogle Scholar
  39. Dynowski M, Mayer M, Moran O, Ludewig U (2008) Molecular determinants of ammonia and urea conductance in plant aquaporin homologs. FEBS Lett 582:2458–2462PubMedCrossRefGoogle Scholar
  40. Eastmond PJ (2004) Glycerol-insensitive Arabidopsis mutants: gli1 seedlings lack glycerol kinase, accumulate glycerol and are more resistant to abiotic stress. Plant J 37:617–625PubMedCrossRefGoogle Scholar
  41. Fischer M, Kaldenhoff R (2008) On the pH regulation of plant aquaporin. J Biol Chem 283:33889–33892PubMedPubMedCentralCrossRefGoogle Scholar
  42. Forrest KL, Bhave M (2008) The PIP and TIP aquaporins in wheat form a large and diverse family with unique gene structures and functionally important features. Funct Integr Genomics 8:115–133PubMedCrossRefGoogle Scholar
  43. Frick A, Järvå M, Törnroth-Horsefield S (2013) Structural basis for pH gating of plant aquaporins. FEBS Lett 587:989–993PubMedCrossRefGoogle Scholar
  44. Froger A, Tallur B, Thomas D, Delamarche C (1998) Prediction of functional residues in water channels and related proteins. Protein Sci 7:1458–1468PubMedPubMedCentralCrossRefGoogle Scholar
  45. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404PubMedPubMedCentralCrossRefGoogle Scholar
  46. George N, Somero GN, Yancey PH (2011) Osmolytes and cell-volume regulation: physiological and evolutionary principles. Handbook of Physiology. Cell Physiol. doi: 10.1002/cphy.cp140110 Google Scholar
  47. Gerber D, Byerrum RU, Gee RW, Tolbert NE (1988) Glycerol concentrations in crop plants. Plant Sciences 56:31–38CrossRefGoogle Scholar
  48. Giovanetti M, Balestrini R, Volpe V, Guether M, Straub D, Costa A, Ludewig U, Bonfante P (2012) Two putative aquaporin genes are differentially expressed during arbuscular mycorrhizal symbiosis in Lotus japonicus. BMC Plant Biol 12:186CrossRefGoogle Scholar
  49. Gomes D, Agasse A, Thiebaud P, Delrot S, Geros H, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 6:1213–1228CrossRefGoogle Scholar
  50. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  51. Gupta AB, 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 Biol 20:134CrossRefGoogle Scholar
  52. Hagel JM, Yeung EC, Facchini PJ (2008) Got milk? The secret life of laticifers. Trends Plant Sci 13:1360–1385CrossRefGoogle Scholar
  53. Hare PD, Cress WA, Van Staen J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553CrossRefGoogle Scholar
  54. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefGoogle Scholar
  55. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42:819–832PubMedCrossRefGoogle Scholar
  56. Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66:300–372PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hove RM, Bhave M (2011) Plant aquaporins with non-aqua functions: deciphering the signature sequences. Plant Mol Biol 75:413–430PubMedCrossRefGoogle Scholar
  58. Jo S, Kim T, Iyer VG, Im W (2008) CHARMM-GUI: a web-based graphical user interface for CHARMM. J Comput Chem 29:1859–1865PubMedCrossRefGoogle Scholar
  59. Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–459PubMedPubMedCentralCrossRefGoogle Scholar
  60. Johansson U, Karlsson M, Johansson I, Gustavsson S, Slovall S, Fraysse L, Weig AR, Kjellbom P (2001) 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 126:1358–1369PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lacote R, Gabla O, Obouayeba S, Eschbach JM, Rivano F, Dian K, Gohet E (2010) Long-term effect of ethylene stimulation on the yield of rubber trees is linked to latex cell biochemistry. Field Crops Res 115:94–98CrossRefGoogle Scholar
  62. Lagree V, Froger A, Deschamps S, Hubert JF, Delamarche C, Bonnec G, Thomas D, Gouranton J, Pellerin I (1999) Switch from an aquaporin to a glycerol channel by two amino acids substitution. J Biol Chem 274:6817–6819PubMedCrossRefGoogle Scholar
  63. Li H, Yunxia Qin Y, Xiao X, Tang C (2011) Screening of valid reference genes for real-time RT-PCR data normalization in Hevea brasiliensis and expression validation of a sucrose transporter gene HbSUT3. Plant Sci 181:132–139PubMedCrossRefGoogle Scholar
  64. Li G, Santoni V, Maurel C (2013) Plant Aquaporins: roles in Plant Physiology. Biochim Biophys Acta 1840:1574–1582PubMedCrossRefGoogle Scholar
  65. Lopez D, Bronner G, Brunel N, Auguin D, Bourgerie S, Brignolas F, Carpin S, Tournaire-Roux C, Maurel C, Fumanal B, Martin F, Sakr S, Label P, Julien JL, Gousset-Dupont A, Venisse JS (2012) Insights into Populus XIP aquaporins: evolutionary expansion, protein functionality, and environmental regulation. J Exp Bot 63:2217–2230PubMedCrossRefGoogle Scholar
  66. Luyten K, Albertyn J, Skibbe WF, Prior BA, Ramos J, Thevelein JM, Hohmann S (1995) Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J 14:1360–1371PubMedPubMedCentralGoogle Scholar
  67. Martins CPS, Pedrosa AM, Du D, Gonçalves LP, Yu Q, Gmitter FG Jr, Costa MGC (2015) Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.). PLoS one 10:e0138786CrossRefGoogle Scholar
  68. Meyrial V, Laize V, Gobin R, Ripoche P, Hohmann S, Tacnet F (2001) Existence of a tightly regulated water channel in Saccharomyces cerevisiae. Eur J Biochem 268:334–343PubMedCrossRefGoogle Scholar
  69. Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin1. Nature 407:599–605PubMedCrossRefGoogle Scholar
  70. Nishimura N, Balch WE (1996) A Di-acidic signal required for selective export from the endoplasmic reticulum. Science 277:556–558CrossRefGoogle Scholar
  71. Nyblom M, Frick A, Wang Y, Ekvall M, Hallgren K, Hedfalk K, Neutze R, Tajkhorshid E, Tornroth-Horsefield S (2009) Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J Mol Biol 387:653–668PubMedCrossRefGoogle Scholar
  72. Obouayeba S, Boa D, Jacob JL (1996) Performance of the PB217 Hevea clone in Cote d’Ivoire. Plant Rech Dev 3:346–354Google Scholar
  73. Pahlman AK, Granath K, Ansell R, Hohmann S, Adler L (2001) The yeast glycerol-3-phosphatases Gpp1p and Gpp2p are required for glycerol biosynthesis and differentially involved in the cellular responses to osmotic, anaerobic, and oxidative stress. J Biol Chem 276:3555–3563PubMedCrossRefGoogle Scholar
  74. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349PubMedCrossRefGoogle Scholar
  75. Park W, Scheffler BE, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol 10:142PubMedPubMedCentralCrossRefGoogle Scholar
  76. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2003–2007CrossRefGoogle Scholar
  77. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: bestKeeper–excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515PubMedCrossRefGoogle Scholar
  78. Prak S, Hem S, Boudet J, Viennois G, Sommerer N, Rossignol M, Maurel C, Santoni V (2008) Multiple phosphorylations in the C-terminal tail of plant membrane aquaporins: role in subcellular trafficking of AtPIP2;1 in response to salt stress. Mol Proteomic 7:1019–1030CrossRefGoogle Scholar
  79. Pujade-Renaud V, Clement A, Perrot-Rechenmann C, Prevot JC, Chrestin H, Jacob JL, Guern J (1994) Ethylene-induced increase in glutamine synthetase activity and mRNA levels in Hevea brasiliensis latex cells. Plant Physiol 105:127–132PubMedPubMedCentralGoogle Scholar
  80. Rahman AYA, Usharraj AO, Misra BB, Thottathil GP, Jayasekaran K, Feng Y et al (2013) Draft genome sequence of the rubber tree Hevea brasiliensis. BMC Genom 14:75CrossRefGoogle Scholar
  81. Reichow SL, Gonen T (2008) Noncanonical binding of calmodulin to aquaporin-0: implications for channel regulation. Structure 16:1389–1398PubMedPubMedCentralCrossRefGoogle Scholar
  82. Reichow SL, Clemens DM, Freites JA, Nemeth-Cahalan KL, Heyden M, Tobias DJ, Hall JE, Gonen T (2013) Allosteric mechanism of water-channel gating by Ca2+-calmodulin. Nat Struct Mol Biol 20:1085–1092PubMedPubMedCentralCrossRefGoogle Scholar
  83. Reuscher S, Akiyama M, Mori C, Aoki K, Shibata D, Shiratake K (2013) Genome-wide identification and expression analysis of aquaporins in tomato. PLoS one 8:e79052PubMedPubMedCentralCrossRefGoogle Scholar
  84. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725–738PubMedPubMedCentralCrossRefGoogle Scholar
  85. Santoni V, Verdoucq L, Sommerer N, Vinh J, Pflieger D, Maurel C (2006) Methylation of aquaporins in plant membrane. Biochem J 400:189–197PubMedPubMedCentralCrossRefGoogle Scholar
  86. Sato K, Nakano A (2007) Mechanisms of COPII vesicle formation and protein sorting. FEBS Lett 581:2076–2082PubMedCrossRefGoogle Scholar
  87. Secchi F, Maciver B, Zeidel ML, Zwieniecki MA (2009) Functional analysis of putative genes encoding the PIP2 water channel subfamily Populus trichocarpa. Tree Physiol 29:1467–1477PubMedCrossRefGoogle Scholar
  88. Sehnal D, Svobodova Varekova R, Berka K, Pravda L, Navratilova V, Banas P, Ionescu CM, Otyepka M, Koca J (2013) MOLE 2.0: advanced approach for analysis of biomacromolecular channels. J Cheminform 5:39PubMedPubMedCentralCrossRefGoogle Scholar
  89. Shen W, Wei Y, Dauk M, Tan Y, Taylor D, Selvaraj G, Zou J (2006) Involvement of glycerol-3-phosphate dehydrogenase ion modulating the NADH/NAD+ ratio provides evidence of a mitochondrial glycerol-3-phosphate shuttle in Arabisopsis. Plant Cell 18:422–441PubMedPubMedCentralCrossRefGoogle Scholar
  90. Sookmark U, Pujade-Renaud V, Chrestin H, Lacote R, Naiyanetr C, Seguin M, Romruensukharom P, Narangajavana J (2002) Characterization of polypeptides accumulated in the latex cytosol of rubber trees affected by the tapping panel dryness syndrome. Plant Cell Physiol 43:1323–1333PubMedCrossRefGoogle Scholar
  91. Soveral G, Madeira A, Loureiro-Dias MC, Moura TF (2007) Water transport in intact yeast cells as assessed by fluorescence self-quenching. Appl Environ Microbiol 73:2341–2343PubMedPubMedCentralCrossRefGoogle Scholar
  92. Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1:2019–2025PubMedCrossRefGoogle Scholar
  93. Sui H, Hana BG, Lee JK, Wallan P, Jap B (2001) structural basis of water-specific transport through the AQP1water channel. Nature 414:872–878PubMedCrossRefGoogle Scholar
  94. Tang CL, Alexov E, Pyle AM, Honig B (2007) Calculation of pKas in RNA: on the structural origins and functional roles of protonated nucleotides. J Mol Biol 366:1475–1496PubMedCrossRefGoogle Scholar
  95. Tang C, Huang D, Yang J, Liu S, Sakr S, Li H, Zhou Y, Quin Y (2010) The sucrose transporter HbSUT3 plays an active role in sucrose loading to laticifer and rubber productivity in exploited trees of Hevea brasiliensis (para rubber tree). Plant Cell Environ 33:1708–1720PubMedCrossRefGoogle Scholar
  96. Tang C, Xiao X, Li H, Fan Y, Yang J, Qi J, Li H (2013) Comparative analysis of latex transcriptome reveals putative molecular mechanisms underlying super productivity of Hevea brasiliensis. PLoS one 8:e75307PubMedPubMedCentralCrossRefGoogle Scholar
  97. Tangphatsornruang S, Uthaipaisanwong P, Sangsrakru D, Chanprasert J, Yoocha T, Jomchai N, Tragoonrung S (2011) Characterization of the complete chloroplast genome of Hevea brasiliensis reveals genome rearrangement, RNA editing sites and phylogenetic relationships. Gene 475:104–112PubMedCrossRefGoogle Scholar
  98. Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439:688–694PubMedCrossRefGoogle Scholar
  99. Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DT, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–397PubMedCrossRefGoogle Scholar
  100. Tungngoen K, Kongsawadworakul P, Viboonjun U, Katsuhara M, Brunel N, Sakr S, Narangajavana J, Chrestin H (2009) Involvement of HbPIP2;1 and HbTIP1;1 aquaporins in ethylene stimulation of latex yield through regulation of water exchanges between inner liber and latex cells in Hevea brasiliensis. Plant Physiol 151:843–856PubMedPubMedCentralCrossRefGoogle Scholar
  101. Tungngoen K, Viboonjun U, Kongsawadworakul P, Katsuhara M, Julien JL, Sakr S, Chrestin H, Narangajavana J (2011) Hormonal treatment of the bark of rubber trees (Hevea brasiliensis) increases latex yield through latex dilution in relation with the differential expression of two aquaporin genes. J Plant Physiol 168:253–262PubMedCrossRefGoogle Scholar
  102. Tupy J (1985) Some aspects of sucrose transport and utilization in latex producing bark of Hevea brasiliensis (Müll. Arg.). Biol Plant 27:51–64CrossRefGoogle Scholar
  103. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74PubMedPubMedCentralCrossRefGoogle Scholar
  104. Vance DE (2001) Phospholipid biosynthesis in eukaryotes. In: Vance DE, Vance JE (eds) Biochemistry of lipids, lipoproteins and membranes (4th edn), vol 8. Elsevier, Amstardam, pp 205–232Google Scholar
  105. Venkatesh J, Yu JW, Park SW (2013) Genome-wide analysis and expression profiling of the Solanum tuberosum aquaporins. Plant Physiol Biochem 73:392–404PubMedCrossRefGoogle Scholar
  106. Venkatesh J, Yu JW, Gastonb D, Park SW (2015) Molecular evolution and functional divergence of X-intrinsic protein genes in plants. Mol Genet Genomics 290:443–460PubMedCrossRefGoogle Scholar
  107. Wallace IC, Roberts DM (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol 135:1059–1068PubMedPubMedCentralCrossRefGoogle Scholar
  108. Webb B, Sali A (2014) Protein structure modeling with MODELLER. Methods Mol Biol 1137:1–15PubMedCrossRefGoogle Scholar
  109. Wei F, Luo S, Zheng Q, Qiu J, Yang W, Wu M, Xiao X (2015) Transcriptome sequencing and comparative analysis reveal long-term flowing mechanisms in Hevea brasiliensis latex. Gene 10:153–162CrossRefGoogle Scholar
  110. Weig AR, Jakob C (2000) Functional identification of the glycerol permease activity of Arabidopsis thaliana NLM1 and NLM2 proteins by heterologous expression in Saccharomyces cerevisiae. FEBS Lett 481:293–298PubMedCrossRefGoogle Scholar
  111. Yang Z, Lasker K, Schneidman-Duhovny D, Webb B, Huang CC, Pettersen EF, Goddard TD, Meng EC, Sali A, Ferrin TE (2012) UCSF Chimera, MODELLER, and IMP: an integrated modeling system. J Struct Biol 179:269–278PubMedCrossRefGoogle Scholar
  112. Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The I-TASSER Suite: protein structure and function prediction. Nat Methods 12:7–8PubMedPubMedCentralCrossRefGoogle Scholar
  113. Yue C, Cao H, Wang L, Zhou Y, Hao X, Zeng J, Wang X, Yang Y (2014) Molecular cloning and expression analysis of tea plant aquaporin (AQP) gene family. Plant Physiol Biochem 83:65–76PubMedCrossRefGoogle Scholar
  114. Zardoya R, Villalba S (2001) A phylogenetic framework for the aquaporin family in eukaryotes. J Mol Evol 52:391–404PubMedGoogle Scholar
  115. Zardoya R, Ding X, Kitagawa Y, Chrispeels MJ (2002) Origin of plant glycerol transporters by horizontal gene transfer and functional recruitment. Proc Natl Acad Sci USA 12:14893–14896CrossRefGoogle Scholar
  116. Zelazny E, Borts JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci USA 104:12359–12364PubMedPubMedCentralCrossRefGoogle Scholar
  117. Zelazny E, Miecielica U, Borst JW, Hemminga MA, Chaumont F (2009) An N-terminal diacidic motif is required for the trafficking of maize aquaporins ZmPIP2;4 and ZmPIP2;5 to the plasma membrane. Plant J 57:346–355PubMedCrossRefGoogle Scholar
  118. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40PubMedPubMedCentralCrossRefGoogle Scholar
  119. Zhang DY, Ali Z, Wang CB, Xu L, Yi JX, Xu ZL, Liu XQ, He XL, Huang YH, Khan IA, Trethowan RM, Ma HX (2013) Genome-wide sequence characterization and expression analysis of major intrinsic proteins in Soybean (Glycine max L.). PLoS one 8:e56312PubMedCentralCrossRefGoogle Scholar
  120. Zhu J, Zhang Z (2009) Ethylene stimulation of latex production in Hevea brasiliensis. Plant Signal Behavior 4:1072–1074CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • David Lopez
    • 1
  • Maroua Ben Amira
    • 1
  • Daniel Brown
    • 2
    • 7
  • Beatriz Muries
    • 3
  • Nicole Brunel-Michac
    • 1
  • Sylvain Bourgerie
    • 4
  • Benoit Porcheron
    • 5
  • Remi Lemoine
    • 5
  • Hervé Chrestin
    • 6
  • Ewan Mollison
    • 7
  • Alessandra Di Cola
    • 7
  • Lorenzo Frigerio
    • 2
  • Jean-Louis Julien
    • 1
  • Aurélie Gousset-Dupont
    • 1
  • Boris Fumanal
    • 1
  • Philippe Label
    • 1
  • Valérie Pujade-Renaud
    • 1
    • 8
  • Daniel Auguin
    • 4
    Email author
  • Jean-Stéphane Venisse
    • 1
    • 9
    Email author
  1. 1.Clermont Université, Université Blaise PascalINRA, UMR 547 PIAF, BP 10448Clermont-FerrandFrance
  2. 2.School of Life SciencesUniversity of WarwickCoventryUK
  3. 3.Institut des Sciences de la VieUniversité catholique de LouvainLouvain-la-NeuveBelgium
  4. 4.Laboratoire de Biologie des Ligneux et des Grandes Cultures, Université d’OrléansUPRES EA 1207, INRA-USC1328OrléansFrance
  5. 5.Ecologie, Biologie des InteractionsEquipe SEVE, UMR 7267 CNRS/Université de PoitiersPoitiers Cedex 9France
  6. 6.Institut de Recherche pour le DéveloppementUR060/CEFE-CNRSMontpellierFrance
  7. 7.Biotechnology Unit, Tun Abdul Razak Research CentreBrickendonburyHertfordUK
  8. 8.CIRAD, UMR AGAPClermont-FerrandFrance
  9. 9.Campus Universitaire des CézeauxAubiere CedexFrance

Personalised recommendations