Early effects of water deficit on two parental clones of Populus nigra grown under different environmental conditions
Claudia Cocozza A B D , Paolo Cherubini B , Nicole Regier B , Matthias Saurer C , Beat Frey B and Roberto Tognetti AA EcoGeoFor Lab, Dipartimento di Scienze e Tecnologie per l’Ambiente e il Territorio (STAT), Università degli Studi del Molise, Contrada Fonte Lappone, I-86090 Pesche, Italy.
B WSL Swiss Federal Institute for Forest, Snow and Landscape Research, Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland.
C PSI Paul Scherrer Institute, CH-5232 Villigen, Switzerland.
D Corresponding author. Email: claudia.cocozza@unimol.it
Functional Plant Biology 37(3) 244-254 https://doi.org/10.1071/FP09156
Submitted: 18 June 2009 Accepted: 22 December 2009 Published: 25 February 2010
Abstract
Global climate change is expected to induce a dramatic increase in the frequency and intensity of drought events in the Mediterranean region. Their effects might be particularly severe in short rotation forestry systems, such as poplar plantations, with high water demands. The aim of this study was to examine the clone-specific reaction of plant-water relations and growth to a dry-down cycle in two parental clones of Populus nigra L.: Poli, which is adapted to the dry/hot climatic conditions of southern Italy, and 58–861, which prefers the cooler and moister conditions typical in northern Italy. Plants were grown in controlled conditions in an airconditioned greenhouse, under three different irrigation regimes for 44 days. Drought stress resulted in a general decrease in plant size and predawn water potential in both clones. Although the control trees grew somewhat taller and retained leaves longer than those in other treatments, the two clones responded differently to water stress. Under severe stress conditions, Poli showed proline accumulation in old leaves to preserve plants from drought damage, without reduced stomatal activity, as shown by low values of δ13C. In 58–861, the accumulation of ABA in roots during drought probably stimulated stomatal control, increasing drought avoidance in this drought-sensitive clone. Although in 58–861 the expression of aquaporin genes PIP1–2 and TIP1–3 was enhanced, in Poli gene expression was downregulated. We analysed only part of the aquaporins genes, but we assume that these clones exhibited contrasting water transport strategies during drought. Clone 58–861 seems to increase the permeability of the vascular tissue by overexpressing aquaporin genes, probably in order to facilitate water transport, and Poli appears to increase water conservation in the root cells by downregulating aquaporins.
Additional keywords: ABA, aquaporins, carbon isotope composition, proline, water stress.
Acknowledgements
Many thanks to Maurizio Sabatti (Università della Tuscia, Viterbo, Italy) for providing the P. nigra cuttings and to Silvia Dingwall for comments on the English language. The work was partially funded by the Swiss Secretariat for Education and Research, COST Action E38 (woody root processes, Grant No. C04.0256). The authors thank the two anonymous reviewers for their helpful comments on the previous version of the manuscript.
Aharon R,
Shahak Y,
Wininger S,
Bendov R,
Kapulnik Y, Galili G
(2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. The Plant Cell 15, 439–447.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ain-Lhout F,
Zunzunegui M,
Diaz Barradas MC,
Tirado R,
Clavijo A, Garcia Novo F
(2001) Comparison of proline accumulation in two mediterranean shrubs subjected to natural and experimental water deficit. Plant and Soil 230, 175–183.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Alexandersson E,
Fraysse L,
Sjövall-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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Arend M, Fromm J
(2007) Seasonal change in the drought response of wood cell development in poplar. Tree Physiology 27, 985–992.
| PubMed |
Barta C, Loreto F
(2006) The relationship between the methyl-erythritol phosphate pathway leading to emission of volatile isoprenoids and abscisic acid content in leaves. Plant Physiology 141, 1676–1683.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bates LS,
Waldren RP, Teare ID
(1973) Rapid determination of free proline water-stress studies. Plant and Soil 39, 205–207.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Betts RA,
Boucher O,
Collins M,
Cox PM, Falloon PD ,
et al
.
(2007) Projected increase in continental runoff due to plant responses to increasing carbon dioxide. Nature 448, 1037–1041.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bogeat-Triboulot MB,
Brosche M,
Renaut J,
Jouve L, Le Thiec D ,
et al
.
(2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiology 143, 876–892.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ceulemans R,
Impens I,
Lemeur R,
Moermans R, Samsuddin Z
(1978) Water movement in the soil-poplar-atmosphere system. I. Comparative study of stomatal morphology and anatomy, and the influence of stomatal density and dimensions on the leaf diffusion characteristics in different poplar clones. Oecologia Plantarum 13, 1–12.
Chen S,
Wang S,
Altman A, Hüttermann A
(1997) Genotypic variation in drought tolerance of poplar in relation to abscisic acid. Tree Physiology 17, 797–803.
| PubMed |
Cochard H,
Ridolfi M, Dreyer E
(1996) Responses to water stress in an ABA- unresponsive hybrid poplar Populus koreana × trichocarpa cv. Peace. II. Hydraulic properties and xylem embolism. New Phytologist 134, 455–461.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Cochard H,
Casella E, Mencuccini M
(2007) Xylem vulnerability to cavitation varies among poplar and willow clones and correlates with yield. Tree Physiology 27, 1761–1767.
| PubMed |
Davies WJ,
Tardieu F, Trejo CL
(1994) How do chemical signals work in plants that grow in drying soil? Plant Physiology 104, 309–314.
|
CAS |
PubMed |
Dickmann DI
(1971) Photosynthesis and respiration by developing leaves of cottonwood (Populus deltoides Bartr.). Botanical Gazette 132, 253–259.
| Crossref | GoogleScholarGoogle Scholar |
Dix PJ, Pearce RS
(1981) Proline accumulation in NaCl-resistant and sensitive cell lines of Nicotiana sylvestris. Zeitschrift fur Pflanzenphysiologie 102, 243–248.
|
CAS |
Farquhar GD,
O’Leary MH, Berry JA
(1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Farquhar GD,
Ehleringer JR, Hubick KT
(1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gaudet M,
Jorge V,
Paolucci I,
Beritognolo I,
Scarascia Mugnozza G, Sabatti M
(2008) Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait. Tree Genetics & Genomes 4, 25–36.
| Crossref | GoogleScholarGoogle Scholar |
Gebre GM, Kuhns MR
(1991) Seasonal and clonal variations in drought tolerance of Populus deltoides. Canadian Journal of Forest Research 21, 910–916.
| Crossref | GoogleScholarGoogle Scholar |
Gebre GM,
Tschaplinski TJ,
Tuskan GA, Todd DE
(1998) Clonal and seasonal differences in leaf osmotic potential and organic solutes of five hybrid clones grown under field conditions. Tree Physiology 18, 645–652.
|
CAS |
PubMed |
Giovannelli A,
Deslauriers A,
Fragnelli G,
Scaletti L,
Castro G,
Rossi S, Crivellaro A
(2007) Evaluation of drought response of two poplar clones Populus × canadensis Mönch ‘I-214’ and P. deltoides Marsh. ‘Dvina’ through high resolution analysis of stem growth. Journal of Experimental Botany 58, 2673–2683.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Griffin DH,
Schaedle M,
Manion PD, Devit M
(1991) Clonal variation in amino acid contents of roots, stems, and leaves of aspen Populus tremuloides Michx. as influenced by diurnal drought stress. Tree Physiology 8, 337–350.
|
CAS |
Hare PD, Cress WA
(1997) Metabolic implications of stress induced proline accumulation in plants. Plant Growth Regulation 21, 79–102.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Harvey HP, van den Driessche R
(1997) Nutrition, xylem cavitation and drought resistance in hybrid poplar. Tree Physiology 17, 647–654.
| PubMed |
Hellemans J,
Mortier G,
De Paepe A,
Speleman F, Vandensompele J
(2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR. Genome Biology 8, R19.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hong Z,
Lakkineni K,
Zhang Z, Verma DPS
(2000) Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiology 122, 1129–1136.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Johnson JD,
Tognetti R, Paris P
(2002) Water relations and gas exchange in poplar and willow under water stress and elevated atmospheric CO2. Physiologia Plantarum 115, 93–100.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kaldenhoff R,
Bertl A,
Otto B,
Moshelion M, Uehlein N
(2007) Characterization of plant aquaporins. Methods in Enzymology 428, 505–531.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Katsuhara M,
Hanba YT,
Shiratake K, Maeshima M
(2008) Expanding roles of plant aquaporins in plasma membranes and cell organelles. Functional Plant Biology 35, 1–14.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Kohler A,
Delaruelle C,
Martin D,
Encelot N, Martin F
(2003) The poplar root transcriptome: analysis of 7000 expressed sequence tags. FEBS Letters 542, 37–41.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liu Z, Dickmann DI
(1992) Abscisic acid accumulation in leaves of two contrasting hybrid poplar clones affected by nitrogen fertilization plus cyclic flooding and soil drying. Tree Physiology 11, 109–122.
|
CAS |
PubMed |
Marjanović Z,
Uehlein N,
Kaldenhoff R,
Zwiazek JJ,
Weiß M,
Hampp R, Nehls U
(2005) Aquaporins in poplar: what a difference a symbiont makes! Planta 222, 258–268.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marron N,
Delay D,
Petit LM,
Dreyer E,
Kahlem G,
Delmotte FM, Brignolas F
(2002) Physiological traits of two Populus × euramericana clones, Luisa Avanzo and Dorskamp, during a water stress and re-watering cycle. Tree Physiology 22, 849–858.
|
CAS |
PubMed |
Marshall JD, Monserud RA
(1996) Homeostatic gas-exchange parameters inferred from 13C/12C in tree rings of conifers. Oecologia 105, 13–21.
| Crossref | GoogleScholarGoogle Scholar |
Monclus R,
Dreyer E,
Villar M,
Delmotte FM,
Delay D,
Petit JM,
Barbaroux C,
Le Thiec D,
Brèchet C, Brignolas F
(2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides × Populus nigra. New Phytologist 169, 765–777.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Montalvo-Hernández L,
Piedra-Ibarra E,
Gómez-Silva L,
Lira-Carmona R,
Acosta-Gallegos JA,
Vazquez-Medrano J,
Xoconostle-Cázares B, Ruíz-Medrano R
(2008) Differential accumulation of mRNAs in drought-tolerant and susceptible common bean cultivars in response to water deficit. New Phytologist 177, 102–113.
| PubMed |
Newton RJ,
Sen S, Puryear JD
(1986) Free proline changes in Pinus taeda L. callus in response to drought stress. Tree Physiology 1, 325–332.
|
CAS |
PubMed |
Pih KT,
Kabilan V,
Lim JH,
Kang SG,
Piao HL,
Jin JB, Hwang I
(1999) Characterization of two new channel protein genes in Arabidopsis. Molecules and Cells 9, 84–90.
|
CAS |
PubMed |
Ramakers C,
Ruijter JM,
Lekanne Deprez RH, Moorman AFM
(2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339, 62–66.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ren J,
Dai W,
Xuan Z,
Yao Y,
Korpelainen H, Li C
(2007) The effect of drought and enhanced UV-B radiation on the growth and physiological traits of two contrasting poplar species. Forest Ecology and Management 239, 112–119.
| Crossref | GoogleScholarGoogle Scholar |
Ridolfi M,
Fauveau ML,
Label P,
Garrec JP, Dreyer E
(1996) Responses to water stress in an ABA-unresponsive hydrid poplar Populus koreana × trichocarpa cv. Peace. I. Stomatal function. New Phytologist 134, 445–454.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Rozen S, Skaletzki H
(2000) Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology (Clifton, N.J.) 132, 365–386.
|
CAS |
PubMed |
Secchi F,
Lovisolo C, Schubert A
(2007) Expression of OePIP2.1 aquaporin gene and water relations of Olea europaea twigs during drought stress and recovery. The Annals of Applied Biology 150, 163–167.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Shvaleva AL,
Silva FCE,
Breia E,
Jouve L,
Hausman JF,
Almeida MH,
Maroco JP,
Rodrigues ML,
Pereira JS, Chaves MM
(2006) Metabolic responses to water deficit in two Eucalyptus globulus clones with contrasting drought sensitivity. Tree Physiology 26, 239–248.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sjödin A,
Street NR,
Sandberg G,
Gustafsson P, Jansson S
(2009) The Populus genome integrative explorer (PopGenIE): a new source for exploring the Populus genome. New Phytologist 182, 1013–1025.
| Crossref | GoogleScholarGoogle Scholar |
Smart LB,
Moskal WA,
Cameron KD, Bennett AB
(2001) MIP genes are down-regulated under drought stress in Nicotiana glauca. Plant & Cell Physiology 42, 686–693.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Souch CA, Stephens W
(1998) Growth, productivity and water use in three hybrid poplar clones. Tree Physiology 18, 829–835.
| PubMed |
Tschaplinski TJ,
Tuskan GA,
Gebre DE, Todd DE
(1998) Drought resistance of two hybrid Populus clones grown in a large-scale plantation. Tree Physiology 18, 653–658.
| PubMed |
Tuskan GA,
DiFazio S,
Jansson S,
Bohlmann J, Grigoriev I ,
et al
.
(2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313, 1596–1604.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Voltas J,
Serrano L,
Hernándezand M, Pemán J
(2006) Carbon isotope discrimination, gas exchange and stem growth of four euramerican hybrid poplars under different watering regimes. New Forests 31, 435–451.
| Crossref | GoogleScholarGoogle Scholar |
Watanabe S,
Kojima K,
Ide Y, Sasaki S
(2000) Effects of saline and osmotic stress on proline and sugar accumulation in Populus euphratica in vitro. Plant Cell, Tissue and Organ Culture 63, 199–206.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Whalley WR,
Clark LJ,
Take WA,
Bird NRA,
Leech PK,
Cope RE, Watts CW
(2007) A porous-matrix sensor to measure the matric potential of soil water in the field. European Journal of Soil Science 58, 18–25.
| Crossref | GoogleScholarGoogle Scholar |
Xu ZZ, Zhou GS
(2006) Nitrogen metabolism and photosynthesis in Leymus chinensis in response to long-term soil drought. Journal of Plant Growth Regulation 25, 252–266.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Yamada S,
Komori T,
Myers PN,
Kuwata S,
Kubo T, Imaseki H
(1997) Expression of plasma membrane water channel genes under water stress in Nicotiana excelsior. Plant & Cell Physiology 38, 1226–1231.
|
CAS |
PubMed |
Yin C,
Duan B,
Wang X, Li C
(2004) Morphological and physiological responses of two contrasting poplar species to drought stress and exogenous abscisic acid application. Plant Science 167, 1091–1097.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Zhang J, Davies WJ
(1987) Increased synthesis of ABA in partially dehydrated root tips and ABA transport from roots to leaves. Journal of Experimental Botany 38, 2015–2023.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Zhang J, Davies WJ
(1990) Changes in the concentration of ABA in xylem sap as a function of changing soil water status com account for changes in leaf conductance and growth. Plant, Cell & Environment 13, 277–285.
| Crossref | GoogleScholarGoogle Scholar |
CAS |