The Hevea brasiliensis XIP aquaporin subfamily: genomic, structural and functional characterizations with relevance to intensive latex harvesting
- 621 Downloads
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.
KeywordsXIP 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.
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.
- 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
- 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
- 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
- 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
- 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
- DeLano WL (2004) PyMOL User’s Guide. DeLano Scientific, San Carlos, p 2004Google Scholar
- Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
- 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
- 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
- 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
- Obouayeba S, Boa D, Jacob JL (1996) Performance of the PB217 Hevea clone in Cote d’Ivoire. Plant Rech Dev 3:346–354Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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