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Early gene expression in the walnut tree occurring during stimulation of leaf hydraulic conductance by irradiance

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Biologia Plantarum

Abstract

Leaf hydraulic conductance (Kleaf) plays a significant part in plant-water regulation. In walnut leaves, Kleaf is stimulated by irradiance and closely relates to the accumulation of JrPIP2s aquaporin transcripts, but it is independent of stomatal aperture. To provide an insight into the early molecular events occurred during light-induced Kleaf, a large-scale transcriptomic analysis consisting of the cDNA-amplified fragment length polymorphism (AFLP) was carried out on walnut leaves maintained under irradiance or in darkness. Of the total 12 000 transcript-derived fragments (TDFs) obtained using cDNA-AFLP with 128 primer pairs, 187 TDFs were selected after sequencing, and only 93 (49 %) that had been ascribed known functions through BLAST searching of the GenBank databases. Most of these TDFs correspond to genes whose protein products are involved in cellular regulation (57.9 %) and global metabolism (39.8 %). To validate cDNA-AFLP expression patterns, 30 TDFs were further analyzed using real-time quantitative polymerase chain reaction. Moreover, exposure of leaves to irradiance was accompanied by the modification of the Ca2+-signaling pathway, ubiquitin-proteasome pathway, vesicle trafficking process and expression of multiple transcription factors.

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Abbreviations

AFLP:

amplified fragment length polymorphism

HPFM:

high pressure flow meter

Kleaf :

leaf hydraulic conductance

Kroot :

root hydraulic conductance

PIP:

plasma membrane intrinsic protein

PCR:

polymerase chain reaction

qRT-PCR:

quantitative real-time PCR

Rleaf :

leaf hydraulic resistance

TDF:

transcript-derived fragment

References

  • Alleva, K., Niemietz, C.M., Maurel, C., Parisi, M., Tyerman, S.D., Amodeo, G.: Plasma membrane of Beta vulgaris storage root shows high water channel activity regulated by cytoplasmic pH and a dual range of calcium concentrations. — J. Exp. Bot. 57: 609–621, 2005.

    Article  Google Scholar 

  • Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W.: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. — Nucl. Acids Res. 25: 3389–3402, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Bachem, C.W., Van der Hoeven, R.S., De Bruijn, S.M., Vreugdenhil, D., Zabeau, A., Visser, R.G.: Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. — Plant J. 9: 745–753, 1995.

    Article  Google Scholar 

  • Baniwal, S.K., Bharti, K., Chan, K.Y., Fauth, M., Ganguli, A., Kotak, S.: Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. — J. Biosci. 29: 471–487, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Ben Baaziz K., Lopez, D., Combes, D., Gousset, A., Bouzid, S., Cochard, H., Sakr, S., Venisse J.S.: Light-mediated K leaf induction and contribution of both the PIP1s and PIP2s aquaporins in five tree species; walnut (Juglans regia) case study. — Tree Physiol., in press, 2012.

  • Brodribb, T.J., Holbrook, N.M.: Diurnal depression of leaf hydraulic conductance in a tropical tree species. — Plant Cell Environ. 27: 820–827, 2004.

    Article  Google Scholar 

  • Brodribb, T.J., Holbrook, N.M., Gutierrez, M.V.: Hydraulic and photosynthetic coordination in seasonally dry tropical forest trees. — Plant Cell Environ. 25: 1435–1444, 2002.

    Article  Google Scholar 

  • Chalhoub, B.A., Thibault, S., Laucou, V., Rameau, C., Hofte, H., Cousin, R.: Silver staining and recovery of AFLP amplification products on large denaturing polyacrylamide gels. — BioTechnology 22: 216–220, 1997.

    CAS  Google Scholar 

  • Chang. S., Puryear, J., Cairney, J.: A simple and efficient method for isolating RNA from pine trees. — Plant mol. Biol. Rep. 11: 113–116, 1993.

    Article  CAS  Google Scholar 

  • Cochard, H., Marton, R., Gross, P., Bogeat-Triboulot, M.B.: Temperature effects on hydraulic conductance and water relations of Quercus robus L. — J. exp. Bot. 51: 1255–1259, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Cochard, H., Venisse, J.S., Barigah, T.S., Brunel, N., Herbette, S., Guilliot, A., Tyree, M.T., Sakr, S.: Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. — Plant Physiol. 143: 122–133, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Cosmstock, J.: Variation in hydraulic architecture and gas exchange in two desert sub-shrubs, Hymenoclea salsola and Ambrosia dumosa. — Oecologia 125: 1–10, 2000.

    Article  Google Scholar 

  • Dhonukshe, P., Aniento, F., Hwang, I., Robinson, D.G., Mravec, J., Stierhof, Y.D., Friml, J.: Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. — Curr. Biol. 17: 520–527, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Du, L., Chen, Z.: Identification of genes encoding receptor-like protein kinases as possible targets of pathogen- and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. — Plant J. 24: 837–847, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Eulgem, T., Rushton, P.J., Schmelzer, E., Hahlbrock, K., Somssich, I.E.: Early nuclear events in plant defence signaling: rapid gene activation by WRKY transcription factors. — EMBO J. 18: 4689–4699, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Evans, J.R., Kaldenhoff, R., Genty, B., Terashima, I.: Resistances along the CO2 diffusion pathway inside leaves. — J. exp. Bot. 60: 2235–2248, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Flexas, J., Diaz-Espejo, A., Galmés, J., Kaldenhoff, R., Medrano, H., Ribas-Carbo, M.: Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. — Plant Cell Environ. 10: 1284–1298, 2007.

    Article  Google Scholar 

  • Frangne, N., Maeshima, M., Schäffner, A.R., Mandel, T., Martinola, E., Bonnemain, J.L.: Expression and distribution of a vacuolar aquaporin in young and mature leaf tissues of Brassica napus in relation to water fluxes. — Planta 212: 270–278, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Fredeen, A., Sage, R.F.: Temperature and humidity effects on branchlet gas-exchange in white spruce: an explanation for the increase in transpiration with branchlet temperature. — Trees 14: 161–168, 1999.

    Article  Google Scholar 

  • Fry, S.C.: Cellulases, hemicelluloses and auxin-stimulated growth: a possible relationship. — Physiol. Plant. 75: 532–536, 1989.

    Article  CAS  Google Scholar 

  • Hachez, C., Heinen, R.B., Draye, X., Chaumont, F.: The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. — Plant mol. Biol. 68: 337–353, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Hayashi, T.: Xyloglucans in the primary cell wall. — Annu. Rev. Plant Physiol. Plant mol. Biol. 40: 139–168, 1989.

    Article  CAS  Google Scholar 

  • Helms, J.B., Zurzolo, C.: Lipids as targeting signals: lipid rafts and intracellular trafficking. — Traffic 5: 247–254, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Hoecker, U.: Regulated proteolysis in light signaling. — Curr. Opin. Plant Biol. 8: 469–476, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Ito, H., Nishitani, K.: Visualization of EXGT-mediated molecular grafting activity by means of a fluorescent-labeled xyloglucan oligomer. — Plant Cell Physiol. 40: 1172–1176, 1999.

    Article  CAS  Google Scholar 

  • Jaillais, Y., Fobis-Loisy, I., Miège, C., Gaude, T.: Evidence for a sorting endosome in Arabidopsis root cells. — Plant J. 53: 237–247, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Johansson, I., Larsson, C., Ek, B., Kjellborm, P.: The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and water potential. — Plant Cell 8: 1181–1191, 1995.

    Google Scholar 

  • Johnson, K.D., Chrispeels, M.J.: Tonoplast-bound protein kinase phosphorylates tonoplast intrinsic protein. — Plant Physiol. 100: 1787–1795, 1992.

    Article  PubMed  CAS  Google Scholar 

  • Kaldenhoff, R., Kölling, A., Meyers, J., Karmann, U., Ruppel, G., Richter, G.: The blue light-responsive AthH2 gene of Arabidopsis thaliana is primarily expressed in expanding as well as in differentiating cells and encodes a putative channel protein of the plasmalemma. — Plant J. 7: 87–95, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Kim, B.H., Schöffl, F.: Interaction between Arabidopsis heat shock transcription factor 1 and 70 kDa heat shock proteins. — J. exp. Bot. 53: 371–375, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Lee, G.J., Vierling, E.: A small heat shock protein cooperates with heat shock protein 70 system to reactivate a heat-denatured protein. — Plant Physiol. 122: 189–197, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Lee, H.K., Cho, S.K., Son, O., Xu, Z., Hwang, I., Kim, W.T.: Drought stress-induced Rma1H1, a RING membraneanchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. — Plant Cell. 21: 622–641, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Leitch, V., Agre, P., King, L.S.: Altered ubiquitination and stability of aquaporin-1 in hypertonic stress. — Proc. nat. Acad. Sci. USA 98: 2894–2898, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Lin, R., Wang, H.: Arabidopsis FHY3/FAR1 gene family and distinct roles of its members in light control of Arabidopsis development. — Plant Physiol. 136: 4010–4022, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. — Methods 25: 402–408, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Lo Gullo, M.A., Nardini, A., Trifolio, P., Salleo, S.: Diurnal and seasonal variations in leaf hydraulic conductance in evergreen and deciduous trees. — Tree Physiol. 25: 505–512, 2005.

    Article  PubMed  Google Scholar 

  • Lu, H.A., Sun, T.X., Matsuzaki, T., Yi, X.H., Eswara, J., Bouley, R.: Heat shock protein 70 interacts with aquaporin-2 and regulates its trafficking. — J. biol. Chem. 282: 28721–28732, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Luan, S., Kudla, J., Rodriguez-Concepcion, M., Yalovsky, S., Gruissem, W.: Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. — Plant Cell 14: 389–400, 2002.

    Google Scholar 

  • Maathuis, F.J., Filatov, V., Herzyk, P., Krijger, G.C., Axelsen, K.B., Chen, S.: Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. — Plant J. 35: 675–692, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Mandadi, K.K., Misra, A., Ren, S., McKnight, T.D.: BT2, a BTB protein, mediates multiple responses to nutrients, stresses, and hormones in Arabidopsis thaliana. — Plant Physiol. 150: 1930–1939, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Matheson, L.A., Suri, S.S., Hanton, S.L., Chatre, L., Brandizzi, F.: Correct targeting of plant ARF GTPases relies on distinct protein domains. — Traffic 9: 103–120, 2008.

    Article  PubMed  CAS  Google Scholar 

  • McCann, M.C., Wells, B., Roberts, K.: Direct visualization of cross-links in the primary plant cell wall. — J. cell. Sci. 96: 323–334, 1990.

    Google Scholar 

  • Nardini, A., Salleo, S.: Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees 15: 14–24, 2000.

    Article  Google Scholar 

  • Nardini, A., Salleo, S.: Water stress-induced modifications of leaf hydraulic architecture in sunflower: co-ordination with gas exchange. — J. exp. Bot. 56: 3093–3101, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Nardini, A., Salleo, S., Raimondo, F.: Changes in leaf hydraulic conductance correlate with leaf vein embolism in Ceris siliquastrum L. — Trees 17: 529–534, 2003.

    Google Scholar 

  • Nardini, A., Tyree, M.T.: Root and shoot hydraulic conductance of seven Quercus species. — Ann. Forest Sci. 56: 371–377, 1999.

    Article  Google Scholar 

  • Negulyaev, Y.A., Vedernikova, E.A., Kinev, A.V., Voronin, A.P.: Exogenous heat shock protein hsp70 activates potassium channels in U937 cells. — Biochem. biophys. Acta 1282: 156–162, 1995.

    Google Scholar 

  • Ng, C.K., Carr, K., McAinsh, M.R., Powell, B., Hetherington, A.M.: Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. — Nature 410: 596–599, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Ooi, C.E., Dell’Angelica, E.C., Bonifacino, J.S.: ADP-ribosylation factor 1 (ARF1) regulates recruitment of the AP-3 adaptor complex to membranes. — J. cell. Biol. 142: 391–402, 1998.

    Article  PubMed  CAS  Google Scholar 

  • Otto, B., Kaldenhoff, R.: Cell-specific expression of the mercury-insensitive plasma-membrane aquaporin NtAQP1 from Nicotiana tabacum. — Planta 211: 167–172, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Paciorek, T., Zazímalová, E., Ruthardt, N., Petrásek, J., Stierhof, Y.D., Kleine-Vehn, J., Morris, D.A., Emans, N., Jürgens, G., Geldner, N., Friml, J.: Auxin inhibits endocytosis and promotes its own efflux from cells. — Nature 435: 1251–1256, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Pandey, S.P., Somssich, I.E.: The role of WRKY transcription factors in plant immunity. — Plant Physiol. 150: 1648–1655, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Ren, S., Mandadi, K.K., Boedeker, A.L., Rathore, K.S., McKnight, T.D.: Regulation of telomerase in Arabidopsis by BT2, an apparent target of TELOMERASE ACTIVATOR1. — Plant Cell 19: 23–31, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Ren, X.-J., Huang, W.-D., Li, W.-Z., Yu, D.-Q.: Tobacco transcription factor WRKY4 is a modulator of leaf development and disease resistance. — Biol. Plant. 54: 684–690, 2010.

    Article  CAS  Google Scholar 

  • Robert, H.S., Quint, A., Brand, D., Vivian-Smith, A., Offringa, R.: BTB and TAZ DOMAIN scaffold proteins perform a crucial function in Arabidopsis development. — Plant J. 58: 109–121, 2008.

    Article  Google Scholar 

  • Rohrbough, J., Rushton, E., Palanker, L., Woodruff, E., Matthies, H., Acharya, U., Acharya, J., Broadie, K.: Ceramidase regulates synaptic vesicle exocytosis and trafficking. — J. Neurosci. 24: 7789–7803, 2003.

    Article  Google Scholar 

  • Sack, L., Holbrook, N.M.: Leaf hydraulics. — Ann. Rev. Plant Biol. 57: 361–381, 2005.

    Article  Google Scholar 

  • Sack, L., Streeter, C.M., Holbrook, N.M.: Hydraulic analysis of water flow through leaves of sugar maple and red oak. — Plant Physiol. 134: 1824–1833, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Sakurai, J., Ahamed, A., Murai, M., Maeshima, M., Uemura, M.: Tissue and cell-specific localization of rice aquaporins and their water transport activities. — Plant Cell Physiol. 49: 30–39, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Sanders, D., Brownlee, C., Harper, J.F.: Communicating with calcium. — Plant Cell 11: 691–706, 1999.

    PubMed  CAS  Google Scholar 

  • Sanders, D., Pelloux, J., Brownlee, C., Harper, J.F.: Calcium at the crossroads of signaling. — Plant Cell 14: 401–417, 2002.

    Google Scholar 

  • Snedden, W.A., Fromm, H.: Calmodulin as a versatile calcium signal transducer in plants. — New Phytol. 151: 35–66, 2002.

    Article  Google Scholar 

  • Thompson, J.E., Smith, R.C., Fry, S.C.: Xyloglucan undergoes interpolymeric transglycosylation during binding to the plant cell wall in vivo: evidence from 13C/3H dual labelling and isopycnic centrifugation in caesium trifluoroacetate. — Biochem. J. 327: 699–708, 1997.

    PubMed  CAS  Google Scholar 

  • Tyree, M.T., Nardini, A., Salleo, S., Sack, L., Bouchra, O.: The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response? — J. exp. Bot. 412: 737–744, 2005.

    Article  Google Scholar 

  • Tyree, M.T., Velez, V., Dalling, K.: Growth dynamics of roots and shoots hydraulic conductance in seedlings of JW five neotropical tree species: scaling to show possible adaptation to differing light regimes. — Oecologia 114: 293–298, 1998.

    Article  Google Scholar 

  • Uehlein, N., Otto, B., Hanson, D.T., Fischer, M., McDowell, N., Kaldenhoff, R.: Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. — Plant Cell 3: 648–657, 2008.

    Google Scholar 

  • Van Wilder, V., Miecielica, U., Degand, H., Derua, R., Waelkens, E., Chaumont, F.: Maize plasma membrane aquaporins belonging to the PIP1 and PIP2 subgroups are in vivo phosphorylated. — Plant Cell Physiol. 49: 1364–1377, 2008.

    Article  PubMed  Google Scholar 

  • Voicu, M.C., Cooke, J.E., Zwiazek, J.J.: Aquaporin gene expression and apoplastic water flow in bur oak (Quercus macrocarpa) leaves in relation to the light response of leaf hydraulic conductance. — J. exp. Bot. 60: 4063–4075, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Vos, P., Hogers, R., Bleeker, M., Reijans, M., Van de Lee, T., Hornes, M.: AFLP: a new technique for DNA fingerprinting. — Nucl. Acids Res. 23: 4407–4414, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Wang, H., Deng, X.W.: Arabidopsis FHY3 defines a key phytochrome A signaling component directly interacting with its homologous partner FAR1. — EMBO J. 21: 1339–1349, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Wang, H., Hao, J., Chen, X., Hao, Z., Wang, X., Lou, Y., Peng, Y., Guo, Z.: Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. — Plant mol. Biol. 65: 799–815, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Wei, W., Zhang, Y., Han, L., Guan, Z., Chai, T.: A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco. — Plant Cell Rep. 27: 795–803, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Worrall, D., Liang, Y.K., Alvarez, S., Holroyd, G.H., Spiegel, S., Panagopulos, M., Gray, J.E., Hetherington, A.M.: Involvement of sphingosine kinase in plant cell signalling. — Plant J. 56: 64–72, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Yang, S., Tyree, M.T.: Hydraulic resistance in Acer saccharum shoots and its influence on leaf water potential and transpiration. — Tree Physiol. 12: 231–242, 1993.

    PubMed  Google Scholar 

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Ben Bâaziz, K., Lopez, D., Bouzid, S. et al. Early gene expression in the walnut tree occurring during stimulation of leaf hydraulic conductance by irradiance. Biol Plant 56, 657–666 (2012). https://doi.org/10.1007/s10535-012-0120-4

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