Comparative study of transcriptional and physiological responses to salinity stress in two contrasting Populus alba L. genotypes.

Soil salinity is an important limiting factor to tree growth and productivity. Populus alba L. is a moderately salt-tolerant species and its natural populations are adapted to contrasting environments, thus providing genetic resources to identify key genes for tolerance to abiotic stress, such as salinity. To elucidate the molecular and genetic basis of variation for salinity tolerance in P. alba, we analyzed the short-term ecophysiological and transcriptome response to salinity. Two contrasting genotypes, 6K3, salt sensitive, and 14P11, salt tolerant, originating from North and South Italy, respectively, were challenged with salt stress (200 mM NaCl). Sodium accumulated in the leaves of salt-treated plants and its concentration increased with time. The net photosynthesis was strongly reduced by salinity in both genotypes, with 6K3 being significantly more affected than 14P11. The transcriptional changes in leaves were analyzed using cDNA microarrays containing about 7000 stress-related poplar expressed sequence tags (EST). A microarray experiment based on RNA pooling showed a number of salinity--regulated transcripts that markedly increased from 3 h to 3 days of salinity treatment. Thus, a detailed analysis was performed on replicated plants collected at 3 days, when ~20% of transcripts showed significant change induced by salinity. In 6K3, there were more genes with decreased expression than genes with increased expression, whereas such a difference was not found in 14P11. Most transcripts with decreased expression were shared between the two genotypes, whereas transcripts with increased expression were mostly regulated in a genotype-specific manner. The commonly decreased transcripts (71 genes) were functionally related to carbohydrate metabolism, energy metabolism and photosynthesis. These biological processes were consistent with the strong inhibition of photosynthesis, caused by salinity. The commonly increased transcripts (13 genes) were functionally related to primary metabolism and biosynthesis of proteins and macromolecules. The salinity-increased transcripts discriminated the molecular response of the two genotypes. In 14P11, the 21 genes specifically salinity-induced were related to stress response, cell development, cell death and catabolism. In 6K3, the 15 genes with salinity-increased expression were involved in protein biosynthesis, metabolism of macromolecules and cell organization and biogenesis. The difference in transcriptome response between the two genotypes could address the molecular basis of intra-specific variation of salinity tolerance in P. alba.

[1]  K. Sailaja,et al.  Ectopic expression of an osmotin gene leads to enhanced salt tolerance in transgenic chilli pepper (Capsicum annum L.) , 2011, Plant Cell, Tissue and Organ Culture (PCTOC).

[2]  P. Khurana,et al.  High-efficiency transformation and selective tolerance against biotic and abiotic stress in mulberry, Morus indica cv. K2, by constitutive and inducible expression of tobacco osmotin , 2011, Transgenic Research.

[3]  N. Tuteja,et al.  Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. , 2010, Plant physiology and biochemistry : PPB.

[4]  D. Hincha,et al.  Faculty Opinions recommendation of Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis. , 2010 .

[5]  A. D. Cullmann,et al.  Linking the Salt Transcriptome with Physiological Responses of a Salt-Resistant Populus Species as a Strategy to Identify Genes Important for Stress Acclimation1[W][OA] , 2010, Plant Physiology.

[6]  R. Ceulemans,et al.  Plasticity of growth and biomass production of an intraspecific Populus alba family grown at three sites across Europe during three growing seasons. , 2010 .

[7]  Lei Yang,et al.  The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress , 2010, Plant Molecular Biology.

[8]  P. Schmitt‐Kopplin,et al.  Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms , 2010, BMC Plant Biology.

[9]  G. Scarascia Mugnozza,et al.  Genetic linkage maps of Populus alba L. and comparative mapping analysis of sex determination across Populus species , 2010, Tree Genetics & Genomes.

[10]  Jian Sun,et al.  H2O2 and cytosolic Ca2+ signals triggered by the PM H-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. , 2010, Plant, cell & environment.

[11]  Wei Sun,et al.  Comparative transcriptomic profiling of a salt-tolerant wild tomato species and a salt-sensitive tomato cultivar. , 2010, Plant & cell physiology.

[12]  F. Mahé,et al.  Transcriptome divergence between the hexaploid salt‐marsh sister species Spartina maritima and Spartina alterniflora (Poaceae) , 2010, Molecular ecology.

[13]  M. Deyholos,et al.  Making the most of drought and salinity transcriptomics. , 2010, Plant, cell & environment.

[14]  A. Hüttermann,et al.  Effect of NaCl on leaf H+-ATPase and the relevance to salt tolerance in two contrasting poplar species , 2010, Trees.

[15]  S. Sensoy,et al.  Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. , 2010, Journal of agricultural and food chemistry.

[16]  F. Sebastiani,et al.  Transcriptome changes in the cambial region of poplar (Populus alba L.) in response to water deficit. , 2010, Plant biology.

[17]  Deqiang Zhang,et al.  Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species , 2010, Plant Molecular Biology.

[18]  A. Polle,et al.  Salinity tolerance of Populus. , 2009, Plant biology.

[19]  J. Schroeder,et al.  HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. , 2009, Trends in plant science.

[20]  S. Zeeman,et al.  Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence. , 2009, Plant, cell & environment.

[21]  G. Mugnozza,et al.  Leaf morphological plasticity and stomatal conductance in three Populus alba L. genotypes subjected to salt stress , 2009 .

[22]  S. Bernard,et al.  The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. , 2009, The New phytologist.

[23]  R. Tanaka,et al.  Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana. , 2009, Plant & cell physiology.

[24]  H. Bohnert,et al.  Transcriptome pathways unique to dehydration tolerant relatives of modern wheat , 2009, Functional & Integrative Genomics.

[25]  C. Sudhakar,et al.  Differential expression of LEA proteins in two genotypes of mulberry under salinity , 2009, Biologia Plantarum.

[26]  Shogo Imada,et al.  Effects of salinity on the growth, Na partitioning, and Na dynamics of a salt-tolerant tree, Populus alba L. , 2009 .

[27]  J. Flexas,et al.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. , 2009, Annals of botany.

[28]  F. A. Rodrigues,et al.  Analysis of gene expression profiles under water stress in tolerant and sensitive sugarcane plants , 2009 .

[29]  T. Flowers,et al.  The ionic effects of NaCl on physiology and gene expression in rice genotypes differing in salt tolerance , 2009, Plant and Soil.

[30]  J. Santamaría,et al.  Incorporation of two trehalose biosynthetic genes in banana increases trehalose levels and protects the photosynthetic apparatus from salt-stress damage , 2009 .

[31]  P. Khurana,et al.  Genetic approaches towards overcoming water deficit in plants - special emphasis on LEAs , 2008, Physiology and Molecular Biology of Plants.

[32]  M. Bonierbale,et al.  Molecular and physiological adaptation to prolonged drought stress in the leaves of two Andean potato genotypes. , 2008, Functional plant biology : FPB.

[33]  Hye Jin Choi,et al.  Differential protection of photosynthetic capacity in trehalose-and lea protein-producing transgenic plants under abiotic stresses , 2008, Journal of Plant Biology.

[34]  R. Tognetti,et al.  Distribution and concentration of cadmium in root tissue of Populus alba determined by scanning electron microscopy and energy-dispersive x-ray microanalysis , 2008 .

[35]  N. Yamanaka,et al.  Growth, photosynthesis, and ion distribution in hydroponically cultured Populus alba L. cuttings grown under various salinity concentrations , 2008, Landscape and Ecological Engineering.

[36]  M. Tester,et al.  Mechanisms of salinity tolerance. , 2008, Annual review of plant biology.

[37]  M. Deyholos,et al.  Transcript expression profile of water-limited roots of hexaploid wheat (Triticum aestivum 'Opata'). , 2008, Genome.

[38]  Norio Murata,et al.  How do environmental stresses accelerate photoinhibition? , 2008, Trends in plant science.

[39]  J. Gray,et al.  Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism , 2008, Proceedings of the National Academy of Sciences.

[40]  R. Azevedo,et al.  Nitrogen use efficiency. 2. Amino acid metabolism , 2007 .

[41]  A. Polle,et al.  Leaf photosynthesis, fluorescence response to salinity and the relevance to chloroplast salt compartmentation and anti-oxidative stress in two poplars , 2007, Trees.

[42]  Jianquan Liu,et al.  Molecular characterization of PeSOS1: the putative Na+/H+ antiporter of Populus euphratica , 2007, Plant Molecular Biology.

[43]  S. Allakhverdiev,et al.  Photoinhibition of photosystem II under environmental stress. , 2007, Biochimica et biophysica acta.

[44]  G. Scarascia Mugnozza,et al.  Functional characterisation of three Italian Populus alba L. genotypes under salinity stress , 2007, Trees.

[45]  Giovanni Parmigiani,et al.  When should one subtract background fluorescence in 2-color microarrays? , 2006, Biostatistics.

[46]  Jianhua Zhu,et al.  The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis , 2006, Proceedings of the National Academy of Sciences.

[47]  C. Hong,et al.  Molecular characterization of theCapsicum annuum RING zinc finger protein 1 (CaRZFP1) gene induced by abiotic stresses , 2006, Journal of Plant Biology.

[48]  A. Mayer Polyphenol oxidases in plants and fungi: going places? A review. , 2006, Phytochemistry.

[49]  D. Chattopadhyay,et al.  Expression of CAP2, an APETALA2-Family Transcription Factor from Chickpea, Enhances Growth and Tolerance to Dehydration and Salt Stress in Transgenic Tobacco1[W] , 2006, Plant Physiology.

[50]  Norio Murata,et al.  A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. , 2006, Biochimica et biophysica acta.

[51]  H. Sixto,et al.  Assessment of salt tolerance in Populus alba clones using chlorophyll fluorescence , 2006, Photosynthetica.

[52]  R. Munns,et al.  Approaches to increasing the salt tolerance of wheat and other cereals. , 2006, Journal of experimental botany.

[53]  T. Chai,et al.  Identification of genes up-regulated in response to Cd exposure in Brassica juncea L. , 2005, Gene.

[54]  P. Auvinen,et al.  Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert , 2005, Genome Biology.

[55]  J. Kangasjärvi,et al.  Populus euphratica Displays Apoplastic Sodium Accumulation, Osmotic Adjustment by Decreases in Calcium and Soluble Carbohydrates, and Develops Leaf Succulence under Salt Stress1[W] , 2005, Plant Physiology.

[56]  H. Bohnert,et al.  Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. , 2005, The Plant journal : for cell and molecular biology.

[57]  R. Bressan,et al.  Unraveling salt tolerance in crops , 2005, Nature Genetics.

[58]  Pascal Condamine,et al.  Comparative Transcriptional Profiling of Two Contrasting Rice Genotypes under Salinity Stress during the Vegetative Growth Stage1[w] , 2005, Plant Physiology.

[59]  Juan Miguel García-Gómez,et al.  BIOINFORMATICS APPLICATIONS NOTE Sequence analysis Manipulation of FASTQ data with Galaxy , 2005 .

[60]  J. Kangasjärvi,et al.  Molecular characterization of PeNhaD1: the first member of the NhaD Na+/H+ antiporter family of plant origin , 2005, Plant Molecular Biology.

[61]  A. Altman,et al.  Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. , 2005, Current opinion in biotechnology.

[62]  Huabo Wang,et al.  Asparagine synthetase gene TaASN1 from wheat is up-regulated by salt stress, osmotic stress and ABA. , 2005, Journal of plant physiology.

[63]  Jill Herschleb,et al.  Functional Analysis of the RING-Type Ubiquitin Ligase Family of Arabidopsis1[w] , 2005, Plant Physiology.

[64]  D. Wolfe,et al.  Suppression of polyphenol oxidases increases stress tolerance in tomato , 2004 .

[65]  S. Strauss,et al.  Validating internal controls for quantitative plant gene expression studies , 2004, BMC Plant Biology.

[66]  T. Sakurai,et al.  Comparative Genomics in Salt Tolerance between Arabidopsis and Arabidopsis-Related Halophyte Salt Cress Using Arabidopsis Microarray1 , 2004, Plant Physiology.

[67]  T. Sharkey,et al.  Diffusive and metabolic limitations to photosynthesis under drought and salinity in C(3) plants. , 2004, Plant biology.

[68]  A. Altman,et al.  Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. , 2004, Trends in plant science.

[69]  Terry Speed,et al.  Normalization of cDNA microarray data. , 2003, Methods.

[70]  Jian-Kang Zhu,et al.  Regulation of Ion Homeostasis under Salt Stress , 2015 .

[71]  M. Rattray,et al.  A model-based analysis of microarray experimental error and normalisation. , 2003, Nucleic acids research.

[72]  A. Altman,et al.  Effects of NaCl on shoot growth, transpiration, ion compartmentation, and transport in regenerated plants of Populus euphratica and Populus tomentosa , 2003 .

[73]  F. Loreto,et al.  Free amino acids and glycine betaine in leaf osmoregulation of spinach responding to increasing salt stress. , 2003, The New phytologist.

[74]  M. Tester,et al.  Na+ tolerance and Na+ transport in higher plants. , 2003, Annals of botany.

[75]  F. Loreto,et al.  Photosynthetic limitations in olive cultivars with different sensitivity to salt stress , 2003 .

[76]  A. Moorman,et al.  Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data , 2003, Neuroscience Letters.

[77]  Yoav Benjamini,et al.  Identifying differentially expressed genes using false discovery rate controlling procedures , 2003, Bioinform..

[78]  A I Saeed,et al.  TM4: a free, open-source system for microarray data management and analysis. , 2003, BioTechniques.

[79]  A. Hüttermann,et al.  Sodium and chloride distribution in roots and transport in three poplar genotypes under increasing NaCl stress , 2002 .

[80]  G. Horgan,et al.  Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR , 2002 .

[81]  A. Sakamoto,et al.  The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. , 2002, Plant, cell & environment.

[82]  B. Black,et al.  Ecotypic and genetic variation in poplar bark storage protein gene expression and accumulation. , 2001, Tree physiology.

[83]  G. Scarascia Mugnozza,et al.  Assessment of geographic variation by RAPD markers among Italian open-pollinated progenies of Populus alba L. , 2001, Genetic Resources and Crop Evolution.

[84]  Michael L. Bittner,et al.  Microarrays: Optical Technologies and Informatics , 2001 .

[85]  Terence P. Speed,et al.  Normalization for cDNA microarry data , 2001, SPIE BiOS.

[86]  A. Altman,et al.  Salt, nutrient uptake and transport, and ABA of Populus euphratica; a hybrid in response to increasing soil NaCl , 2001, Trees.

[87]  J. Moroney,et al.  Carbonic anhydrases in plants and algae , 2001 .

[88]  C. P. Constabel,et al.  Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. , 2000, Plant physiology.

[89]  E. Blumwald Sodium transport and salt tolerance in plants. , 2000, Current opinion in cell biology.

[90]  H. Shi,et al.  The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Kubo,et al.  Differential expression of plastidic aldolase genes in Nicotiana plants under salt stress. , 2000, Plant science : an international journal of experimental plant biology.

[92]  E. Blumwald,et al.  Sodium transport in plant cells. , 2000, Biochimica et biophysica acta.

[93]  D. Yakir,et al.  Internal Conductance to CO2 Diffusion and C18OO Discrimination in C3 Leaves , 2000 .

[94]  Villani,et al.  Restrictions to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress , 1999, Plant physiology.

[95]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[96]  C. Rice-Evans,et al.  Antioxidant properties of phenolic compounds , 1997 .

[97]  J. Cairney,et al.  A simple and efficient method for isolating RNA from pine trees , 1993, Plant Molecular Biology Reporter.

[98]  P. Hasegawa,et al.  Characterization of osmotin : a thaumatin-like protein associated with osmotic adaptation in plant cells. , 1987, Plant physiology.

[99]  S. K. Boey,et al.  Plasma Membrane , 2005 .

[100]  S. Mathur,et al.  Chlorophyll a fluorescence study revealing effects of high salt stress on Photosystem II in wheat leaves. , 2010, Plant physiology and biochemistry : PPB.

[101]  N. Yamanaka,et al.  Responses to nonaeration and/or salinity stress in hydroponically cultured Populus nigra and Populus alba cuttings , 2009, Landscape and Ecological Engineering.

[102]  R. Pérez-Vicente,et al.  Expression of asparagine synthetase genes in sunflower (Helianthus annuus) under various environmental stresses. , 2007, Plant physiology and biochemistry : PPB.

[103]  G. Chirici,et al.  MODELLO DI VALUTAZIONE DELL'ATTITUDINE FISICA DEL TERRITORIO PER LA REALIZZAZIONE DI IMPIANTI CEDUI DA BIOMASSA IN ITALIA ( 1 ) , 2007 .

[104]  H. Sixto,et al.  Response to sodium chloride in different species and clones of genus Populus L. , 2005 .

[105]  Giovanni Parmigiani,et al.  When Should One Substract Background Fluorescence in Two Color Microarrays , 2005 .

[106]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[107]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[108]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[109]  Malhotra Sk,et al.  The plasma membrane , 1988 .