Exploring Picea glauca aquaporins in the context of needle water uptake and xylem refilling

New Phytologist

Volumn 203, Issue 2, 2014, Pages 388-400

  Laur, Joan ^a   Hacke, Uwe G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Aquaporins; Endodermis; Foliar water uptake; Picea glauca; Plasma membrane intrinsic proteins (PIPs); Radial water flow; Xylem refilling

Indexed keywords

CELL ORGANELLE; CONIFEROUS TREE; DROUGHT STRESS; PHYSIOLOGY; WATER UPTAKE; XYLEM;

CONIFEROPHYTA; PICEA; PICEA GLAUCA; PIPS;

AQUAPORIN; VEGETABLE PROTEIN;

ANATOMY AND HISTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MULTIGENE FAMILY; PHYLOGENY; PHYSIOLOGY; PLANT LEAF; PLANT STEM; PLANT STOMA; REAL TIME POLYMERASE CHAIN REACTION; SPRUCE; XYLEM;

AQUAPORINS; GENE EXPRESSION REGULATION, PLANT; MULTIGENE FAMILY; PHYLOGENY; PICEA; PLANT LEAVES; PLANT PROTEINS; PLANT STEMS; PLANT STOMATA; REAL-TIME POLYMERASE CHAIN REACTION; XYLEM;

EID: 84902545630     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12806     Document Type: Article

References (70)

1. Alba R, Fei Z, Payton P, Liu Y, Moore SL, Debbie P, Cohn J, D'Ascenzo M, Gordon JS, Rose JKC et al. 2004. ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant Journal 39: 697-714.
2. Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P. 2005. Whole gene family expression and drought stress regulation of aquaporins. Plant Molecular Biology 59: 469-484.
3. Almeida-Rodriguez AM, Hacke UG, Laur J. 2011. Influence of evaporative demand on aquaporin expression and root hydraulics in hybrid poplar. Plant, Cell & Environment 34: 1318-1331.
4. Altschul SF, Madden TL, Schäffer 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 Research 25: 3389-3402.
5. Arvidsson S, Kwasniewski M, Riano-Pachon D, Mueller-Roeber B. 2008. QuantPrime - a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics 9: 465.
6. Begg JE, Turner NC. 1970. Water potential gradients in field tobacco. Plant Physiology 46: 343-346.
7. Birol I, Raymond A, Jackman SD, Pleasance S, Coope R, Taylor GA, Saint Yuen MM, Keeling CI, Brand D, Vandervalk BP et al. 2013. Assembling the 20 Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data. Bioinformatics 29: 1492-1497.
8. Boucher JF, Munson AD, Bernier PY. 1995. Foliar absorption of dew influences shoot water potential and root-growth in Pinus strobus seedlings. Tree Physiology 15: 819-823.
9. Braissant O, Wahli W. 1998. A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1: 10-16.
10. Breshears DD, McDowell NG, Goddard KL, Dayem KE, Martens SN, Meyer CW, Brown KM. 2008. Foliar absorption of intercepted rainfall improves woody plant water status most during drought. Ecology 89: 41-47.
11. Burgess SSO, Dawson TE. 2004. The contribution of fog to the water relations of Sequoia sempervirens (D. Don): foliar uptake and prevention of dehydration. Plant, Cell & Environment 27: 1023-1034.
12. Burkhardt J. 2010. Hygroscopic particles on leaves: nutrients or desiccants? Ecological Monographs 80: 369-399.
13. Burkhardt J, Basi S, Pariyar S, Hunsche M. 2012. Stomatal penetration by aqueous solutions - an update involving leaf surface particles. New Phytologist 196: 774-787.
14. Chang S, Puryear J, Cairney J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11: 113-116.
15. Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R. 2001. Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiology 125: 1206-1215.
16. Chou K-C, Shen H-B. 2010. Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5: e11335.
17. Claros MG, von Heijne G. 1994. TopPred-II - an improved software for membrane-protein structure predictions. Computer Applications in the Biosciences 10: 685-686.
18. Clifford SC, Arndt SK, Popp M, Jones HG. 2002. Mucilages and polysaccharides in Ziziphus species (Rhamnaceae): localization, composition and physiological roles during drought-stress. Journal of Experimental Botany 53: 131-138.
19. Daniels MJ, Mirkov TE, Chrispeels MJ. 1994. The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiology 106: 1325-1333.
20. Danielson J, Johanson U. 2008. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biology 8: 45.
21. Eller CB, Lima AL, Oliveira RS. 2013. Foliar uptake of fog water and transport belowground alleviates drought effects in the cloud forest tree species, Drimys brasiliensis (Winteraceae). New Phytologist 199: 151-162.
22. Fouquet R, Léon C, Ollat N, Barrieu F. 2008. Identification of grapevine aquaporins and expression analysis in developing berries. Plant Cell Reports 27: 1541-1550.
23. Fraysse LC, Wells B, McCann MC, Kjellbom P. 2005. Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells. Biology of the Cell 97: 519-534.
24. Goldsmith GR. 2013. Changing directions: the atmosphere-plant-soil continuum. New Phytologist 199: 4-6.
25. Goldsmith GR, Matzke NJ, Dawson TE. 2013. The incidence and implications of clouds for cloud forest plant water relations. Ecology Letters 16: 307-314.
26. Gomes D, Agasse A, Thiébaud P, Delrot S, Gerós H, Chaumont F. 2009. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochimica et Biophysica Acta (BBA) - Biomembranes 1788: 1213-1228.
27. Gong HQ, Peng YB, Zou C, Wang DH, Xu ZH, Bai SN. 2006. A simple treatment to significantly increase signal specificity in immunohistochemistry. Plant Molecular Biology Reporter 24: 93-101.
28. Gotsch SG, Asbjornsen H, Holwerda F, Goldsmith GR, Weintraub AE, Dawson TE. 2014. Foggy days and dry nights determine crown-level water balance in a seasonal tropical montane cloud forest. Plant, Cell & Environment 37: 261-272.
29. 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 Biology 9: 134.
30. Hachez C, Heinen RB, Draye X, Chaumont F. 2008. The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Molecular Biology 68: 337-353.
31. Hacke UG, Jansen S. 2009. Embolism resistance of three boreal conifer species varies with pit structure. New Phytologist 182: 675-686.
32. Hakman I, Oliviusson P. 2002. High expression of putative aquaporin genes in cells with transporting and nutritive functions during seed development in Norway spruce (Picea abies). Journal of Experimental Botany 53: 639-649.
33. Heinen RB, Ye Q, Chaumont F. 2009. Role of aquaporins in leaf physiology. Journal of Experimental Botany 60: 2971-2985.
34. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. 2007. WoLF PSORT: protein localization predictor. Nucleic Acids Research 35: W585-W587.
35. Huang XQ, Madan A. 1999. CAP3: a DNA sequence assembly program. Genome Research 9: 868-877.
36. Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall 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 Physiology 126: 1358-1369.
37. Kammerloher W, Fischer U, Piechottka GP, Schäffner AR. 1994. Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant Journal 6: 187-199.
38. Karlgren A, Carlsson J, Gyllenstrand N, Lagercrantz U, Sundström JF. 2009. Non-radioactive in situ hybridization protocol applicable for Norway spruce and a range of plant species. Journal of Visualized Experiments 26: 1205.
39. Katz C, Oren R, Schulze ED, Milburn JA. 1989. Uptake of water and solutes through twigs of Picea abies (L.) Karst. Trees 3: 33-37.
40. Laur J, Hacke UG. 2013. Transpirational demand affects aquaporin expression in poplar roots. Journal of Experimental Botany 64: 2283-2293.
41. Liesche J, Martens HJ, Schulz A. 2011. Symplasmic transport and phloem loading in gymnosperm leaves. Protoplasma 248: 181-190.
42. Limm EB, Simonin KA, Bothman AG, Dawson TE. 2009. Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. Oecologia 161: 449-459.
43. Maurel C, Verdoucq L, Luu DT, Santoni V. 2008. Plant aquaporins: membrane channels with multiple integrated functions. Annual Review of Plant Biology 59: 595-624.
44. Mayr S, Schmid P, Laur J, Rosner S, Charra-Vaskou K, Daemon B, Hacke UG. 2014. Uptake of water via branches helps timberline conifers refill embolized xylem in late winter. Plant Physiology 164: 114.
45. McCulloh KA, Johnson DM, Meinzer FC, Lachenbruch B. 2011. An annual pattern of native embolism in upper branches of four tall conifer species. American Journal of Botany 98: 1007-1015.
46. Nadezhdina N, David TS, David JS, Ferreira MI, Dohnal M, Tesař M, Gartner K, Leitgeb E, Nadezhdin V, Cermak J et al. 2010. Trees never rest: the multiple facets of hydraulic redistribution. Ecohydrology 3: 431-444.
47. Nardini A, Lo Gullo MA, Salleo S. 2011. Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Science 180: 604-611.
48. Néron B, Ménager H, Maufrais C, Joly N, Maupetit J, Letort S, Carrere S, Tuffery P, Letondal C. 2009. Mobyle: a new full web bioinformatics framework. Bioinformatics 25: 3005-3011.
49. North GB, Lynch FH, Maharaj FDR, Phillips CA, Woodside WT. 2013. Leaf hydraulic conductance for a tank bromeliad: axial and radial pathways for moving and conserving water. Frontiers in Plant Science 4: 78.
50. Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A et al. 2013. The Norway spruce genome sequence and conifer genome evolution. Nature 497: 579-584.
51. Ohrui T, Nobira H, Sakata Y, Taji T, Yamamoto C, Nishida K, Yamakawa T, Sasuga Y, Yaguchi Y, Takenaga H et al. 2007. Foliar trichome- and aquaporin-aided water uptake in a drought-resistant epiphyte Tillandsia ionantha Planchon. Planta 227: 47-56.
52. Oliveira RS, Dawson TE, Burgess SSO. 2005. Evidence for direct water absorption by the shoot of the desiccation-tolerant plant Vellozia flavicans in the savannas of central Brazil. Journal of Tropical Ecology 21: 585-588.
53. Oliviusson P, Salaj J, Hakman I. 2001. Expression pattern of transcripts encoding water channel-like proteins in Norway spruce (Picea abies). Plant Molecular Biology 46: 289-299.
54. Pavy N, Boyle B, Nelson C, Paule C, Giguere I, Caron S, Parsons LS, Dallaire N, Bedon F, Berube H et al. 2008. Identification of conserved core xylem gene sets: conifer cDNA microarray development, transcript profiling and computational analyses. New Phytologist 180: 766-786.
55. Plavcová L, Hacke UG. 2012. Phenotypic and developmental plasticity of xylem in hybrid poplar saplings subjected to experimental drought, nitrogen fertilization, and shading. Journal of Experimental Botany 63: 6481-6491.
56. Rice P, Bleasby A, Ison J, Uludag M. 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends in Genetics 16: 276-277.
57. Rigault P, Boyle B, Lepage P, Cooke JEK, Bousquet J, MacKay JJ. 2011. A white spruce gene catalog for conifer genome analyses. Plant Physiology 157: 14-28.
58. Romualdi C, Bortoluzzi S, D'Alessi F, Danieli GA. 2003. IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiological Genomics 12: 159-162.
59. Rutledge RG, Stewart D. 2010. Assessing the performance capabilities of LRE-based assays for absolute quantitative real-time PCR. PLoS ONE 5: e9731.
60. Sakurai-Ishikawa J, Murai-Hatano M, Hayashi H, Ahamed A, Fukushi K, Matsumoto T, Kitagawa Y. 2011. Transpiration from shoots triggers diurnal changes in root aquaporin expression. Plant, Cell & Environment 34: 1150-1163.
61. Sauter J, Dörr I, Kollmann R. 1976. The ultrastructure of Strasburger cells (= albuminous cells) in the secondary phloem of Pinus nigra var. austriaca (Hoess) Badoux. Protoplasma 88: 31-49.
62. Schoonmaker AL, Hacke UG, Landhausser SM, Lieffers VJ, Tyree MT. 2010. Hydraulic acclimation to shading in boreal conifers of varying shade tolerance. Plant. Cell & Environment 33: 382-393.
63. Shatil-Cohen A, Attia Z, Moshelion M. 2011. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant Journal 67: 72-80.
64. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li WZ, Lopez R, McWilliam H, Remmert M, Soding J et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7: 539.
65. Simonin KA, Santiago LS, Dawson TE. 2009. Fog interception by Sequoia sempervirens (D. Don) crowns decouples physiology from soil water deficit. Plant, Cell & Environment 32: 882-892.
66. Sparks JP, Campbell GS, Black RA. 2001. Water content, hydraulic conductivity, and ice formation in winter stems of Pinus contorta: a TDR case study. Oecologia 127: 468-475.
67. Sperry JS, Donnelly JR, Tyree MT. 1988. A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment 11: 35-40.
68. Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE. 1994. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75: 1736-1752.
69. Thompson JD, Plewniak F, Ripp R, Thierry JC, Poch O. 2001. Towards a reliable objective function for multiple sequence alignments. Journal of Molecular Biology 314: 937-951.
70. Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD. 2009. The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiology 149: 445-460.