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

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Abstract

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.

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Acknowledgments

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.

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Authors and Affiliations

  1. Clermont Université, Université Blaise Pascal, INRA, UMR 547 PIAF, BP 10448, 63000, Clermont-Ferrand, France

    David Lopez, Maroua Ben Amira, Nicole Brunel-Michac, Jean-Louis Julien, Aurélie Gousset-Dupont, Boris Fumanal, Philippe Label, Valérie Pujade-Renaud & Jean-Stéphane Venisse

  2. School of Life Sciences, University of Warwick, Coventry, CV4 7AL, UK

    Daniel Brown & Lorenzo Frigerio

  3. Institut des Sciences de la Vie, Université catholique de Louvain, 1348, Louvain-la-Neuve, Belgium

    Beatriz Muries

  4. Laboratoire de Biologie des Ligneux et des Grandes Cultures, Université d’Orléans, UPRES EA 1207, INRA-USC1328, 45067, Orléans, France

    Sylvain Bourgerie & Daniel Auguin

  5. Ecologie, Biologie des Interactions, Equipe SEVE, UMR 7267 CNRS/Université de Poitiers, Bâtiment B31, TSA 51106, 86073, Poitiers Cedex 9, France

    Benoit Porcheron & Remi Lemoine

  6. Institut de Recherche pour le Développement, UR060/CEFE-CNRS, 1029 route de Mende, 34032, Montpellier, France

    Hervé Chrestin

  7. Biotechnology Unit, Tun Abdul Razak Research Centre, Brickendonbury, Hertford, UK

    Daniel Brown, Ewan Mollison & Alessandra Di Cola

  8. CIRAD, UMR AGAP, 63000, Clermont-Ferrand, France

    Valérie Pujade-Renaud

  9. Campus Universitaire des Cézeaux, 8 Avenue Blaise Pascal, TSA 60026, CS 60026, 63178, Aubiere Cedex, France

    Jean-Stéphane Venisse

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  1. David Lopez
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Electronic supplementary material

Below is the link to the electronic supplementary material.

11103_2016_462_MOESM1_ESM.docx

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

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

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

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

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

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

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

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

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)

Supplementary Fig. S10 High-definition format of Fig. 2 (PPTX 11205 kb)

11103_2016_462_MOESM11_ESM.xlsx

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

Supplementary Tab. S2 Primers used for qPCR amplification, in situ hybridization, yeast experiments and ectopic expressions in tobacco (XLSX 13 kb)

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Lopez, D., Amira, M.B., Brown, D. et al. The Hevea brasiliensis XIP aquaporin subfamily: genomic, structural and functional characterizations with relevance to intensive latex harvesting. Plant Mol Biol 91, 375–396 (2016). https://doi.org/10.1007/s11103-016-0462-y

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