Structural and functional characterisation of two novel durum wheat annexin genes in response to abiotic stress
Marwa Harbaoui A , Rania Ben Saad A , Nihed Ben Halima B , Mouna Choura A and Faiçal Brini A C
+ Author Affiliations
- Author Affiliations
A Biotechnology and Plant Improvement Laboratory, Centre of Biotechnology of Sfax, University of Sfax, B.P “1177” 3018, Sfax,Tunisia.
B Faculty of Medicine of Sfax, University of Sfax, Sfax-Tunisia.
C Corresponding author. Email: faical.brini@cbs.rnrt.tn
Functional Plant Biology 45(5) 542-552 https://doi.org/10.1071/FP17212
Submitted: 26 July 2017 Accepted: 12 November 2017 Published: 14 December 2017
Abstract
Abiotic stress results in massive loss of crop productivity throughout the world. Understanding the plant gene regulatory mechanisms involved in stress responses is very important. Annexins are a conserved multigene family of Ca-dependent, phospholipid-binding proteins with suggested functions in response to environmental stresses and signalling during plant growth and development. Annexins function to counteract oxidative stress, maintain cell redox homeostasis and enhance drought tolerance. A full-length cDNA of two genes (TdAnn6 and TdAnn12) encoding annexin proteins were isolated and characterised from Tunisian durum wheat varieties (Triticum turgidum L. subsp. durum cv. Mahmoudi). Analyses of the deduced proteins encoded by annexin cDNAs (TdAnn6 and TdAnn12) indicate the presence of the characteristic four repeats of 70–75 amino acids and the motifs proposed to be involved in Ca2+ binding. Gene expression patterns obtained by real-time PCR revealed differential temporal and spatial regulation of the two annexin genes in durum wheat under different abiotic stress conditions such as salt (NaCl 150 mM), osmotic (10% polyethylene glycol 8000), ionic (LiCl 10 mM), oxidative (H2O2), ABA (100 µM), salicylic acid (10 mM), cold (4°C) and heat (37°C) stress. The two annexin genes were not regulated by heavy metal stress (CdCl2 150 µM). Moreover, heterologous expression of TdAnn6 and TdAnn12 in yeast improves its tolerance to abiotic stresses, suggesting annexin’s involvement in theses stress tolerance mechanisms. Taken together, our results show that the two newly isolated wheat annexin might play an active role in modulating plant cell responses to abiotic stress responses.
Additional keywords: abiotic stress tolerance, phylogenetic analysis, yeast.
References
Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schaffer AA, Yu YK (2005) Protein database searches using compositionally adjusted substitution matrices. The FEBS Journal 272, 5101–5109.| Protein database searches using compositionally adjusted substitution matrices.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGqtbvF&md5=499f5b0d459865b338feb84ba5273a8eCAS |
Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In ‘Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology’. pp. 28–36. (AAAI Press, Menlo Park, California)
Bailey TL, Gribskov M (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14, 48–54.
| Combining evidence using p-values: application to sequence homology searches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFygs78%3D&md5=23d4f24c4adf2061ce8e4573c6208366CAS |
Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Research 43, W39–W49.
| The MEME suite.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtVymtbrO&md5=f1e93064ea675c2f3128bb02d58fda94CAS |
Bairoch A, Apweiler R, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, Donovan CO, Redaschi N, Yeh LS (2005) The Universal Protein Resource (UniProt). Nucleic Acids Research 33, D154–D159.
| The Universal Protein Resource (UniProt).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisVCktg%3D%3D&md5=27365eca18df3e6eb5e2801204ba63f4CAS |
Bassani M, Neumann PM, Gepstein S (2004) Differential expression profiles of growth-related genes in the elongation zone of maize primary roots. Plant Molecular Biology 56, 367–380.
Baucher M, Oukouomi Lowe Y, Vandeputte OM, Mukoko Bopopi J, Moussawi J, Vermeersch M, Mol A, El Jaziri M, Homblé F, Pérez-Morga D (2011) Ntann12 annexin expression is induced by auxin in tobacco roots. Journal of Experimental Botany 62, 4055–4065.
| Ntann12 annexin expression is induced by auxin in tobacco roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFGjsLg%3D&md5=d51a05a6b5b2394b8540cf8a6736fb5fCAS |
Bharadwaj A, Bydoun M, Holloway R, Waisman D (2013) Annexin A2 heterotetramer: structure and function. International Journal of Molecular Sciences 14, 6259–6305.
| Annexin A2 heterotetramer: structure and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlt1Gju74%3D&md5=fa83cb32c5bae59f222ae4e0d5bc33a9CAS |
Botella JR, Arteca RN (1994) Differential expression of 2 calmodulin genes in response to physical and chemical stimuli. Plant Molecular Biology 24, 757–766.
| Differential expression of 2 calmodulin genes in response to physical and chemical stimuli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFSjurg%3D&md5=96d24178f59ff85f00301a1dc1b028e6CAS |
Breton G, Vazquez Tello A, Danyluk J, Sarhan F (2000) Two novel intrinsic annexins accumulate in wheat membranes in response to low temperature. Plant & Cell Physiology 41, 177–184.
| Two novel intrinsic annexins accumulate in wheat membranes in response to low temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtlyhs7k%3D&md5=7955cee2ef16fbca5612970a51522d67CAS |
Chu P, Chen H, Zhou Y, Li Y, Ding Y, Jiang L, Tsang EW, Wu K, Huang S (2012) Proteomic and functional analyses of Nelumbo nucifera annexins involved in seed thermotolerance and germination vigor. Planta 235, 1271–1288.
| Proteomic and functional analyses of Nelumbo nucifera annexins involved in seed thermotolerance and germination vigor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnslams7k%3D&md5=1f503e03294ae2dbaa7dfd8ea4645216CAS |
Clark GB, Dauwalder M, Roux SJ (1998) Immunological and biochemical evidence for nuclear localization of annexin in peas. Plant Physiology and Biochemistry 36, 621–627.
| Immunological and biochemical evidence for nuclear localization of annexin in peas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvVyjtrw%3D&md5=9336497dbbb0b650d4b1f66012df25a4CAS |
Clark GB, Sessions A, Eastburn DJ, Roux SJ (2001) Differential expression of members of the annexin multigene family in Arabidopsis. Plant Physiology 126, 1072–1084.
| Differential expression of members of the annexin multigene family in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVarur0%3D&md5=ee17cfc065ac1ee5da8be345e1d8883eCAS |
Clark GB, Morgan RO, Fernandez MP, Roux SJ (2012) Evolutionary adaptation of plant annexins has diversified their molecular structures, interactions and functional roles. New Phytologist 196, 695–712.
| Evolutionary adaptation of plant annexins has diversified their molecular structures, interactions and functional roles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVKrt7vL&md5=8251408bc83d5269f0e791149db70883CAS |
De Carvalho-Niebel F, Timmers AC, Chabaud M, Defaux-Petras A, Barker DG (2002) The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula. The Plant Journal 32, 343–352.
| The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt12ms74%3D&md5=12745791bd64696a78dbe2133f13d989CAS |
DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signaling. The Biochemical Journal 425, 27–40.
| Breaking the code: Ca2+ sensors in plant signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Sru7vM&md5=ddf61a29ac3e79995cb397a89f37c951CAS |
Divya K, Jami SK, Kirti PB (2010) Constitutive expression of mustard annexin, AnnBj1 enhances abiotic stress tolerance and fiber quality in cotton under stress. Plant Molecular Biology 73, 293–308.
| Constitutive expression of mustard annexin, AnnBj1 enhances abiotic stress tolerance and fiber quality in cotton under stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFKqsbg%3D&md5=22d451a04a1036c2b6d39b844ed09b4bCAS |
Elble R (1992) A simple and efficient procedure for transformation of yeasts. BioTechniques 13, 18–20.
Epstein E (1972) ‘Mineral nutrition of plants: Principles and perspectives.’ (John Wiley and Sons, New York)
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Research 42, D222–D230.
| Pfam: the protein families database.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXos1al&md5=7a0b6c011fa59b0291d4e33bf1d7cd4cCAS |
Gao Y, Gillen CM, Wheatly MG (2009) Cloning and characterization of a calmodulin gene (CaM) in crayfish Procambarus clarkii and expression during molting. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 152, 216–225.
| Cloning and characterization of a calmodulin gene (CaM) in crayfish Procambarus clarkii and expression during molting.Crossref | GoogleScholarGoogle Scholar |
Gerke V, Moss SE (2002) Annexins: from structure to function. Physiological Reviews 82, 331–371.
| Annexins: from structure to function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFOns7c%3D&md5=05913dd0b9d09f20ed8f1993ceb0f6e3CAS |
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. The Plant Journal 61, 1041–1052.
| Research on plant abiotic stress responses in the post-genome era: past, present and future.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvFKntL4%3D&md5=622bcfb3d3f920f576acb0d5da0098d7CAS |
Hofmann A, Proust J, Dorowski A, Schantz R, Huber R (2000) Annexin 24 from Capsicum annuum: X-ray structure and biochemical characterization. The Journal of Biological Chemistry 275, 8072–8082.
| Annexin 24 from Capsicum annuum: X-ray structure and biochemical characterization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitVyltLk%3D&md5=e48e8e37680301b9edb6955ed852ca96CAS |
Hu NJ, Yusof AM, Winter A, Osman A, Reeve AK, Hofmann A (2008) The crystal structure of calcium-bound annexin Gh1 from Gossypium hirsutum and its implications for membrane binding mechanisms of plant annexins. The Journal of Biological Chemistry 283, 18314–18322.
| The crystal structure of calcium-bound annexin Gh1 from Gossypium hirsutum and its implications for membrane binding mechanisms of plant annexins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVCnsbo%3D&md5=742c418dae5a4b733cfe80f839a04417CAS |
Huang Y, Wang J, Zhang L, Zuo K (2013) A cotton annexin protein AnxGb6 regulates fiber elongation through its interaction with actin 1. PLoS One 8, e66160
| A cotton annexin protein AnxGb6 regulates fiber elongation through its interaction with actin 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFWntbk%3D&md5=54c56f649f81dcb7245b05ca8303a3c6CAS |
Huh SM, Noh EK, Kim HG, Jeon BW, Bae K, Hu HC, Kwak JM, Park OK (2010) Arabidopsis annexins AnnAt1 and AnnAt4 interact with each other and regulate drought and salt stress responses. Plant & Cell Physiology 51, 1499–1514.
| Arabidopsis annexins AnnAt1 and AnnAt4 interact with each other and regulate drought and salt stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFyltLrM&md5=d0b47cecb9be2362710fd2f1ea3626acCAS |
Jami SK, Clark GB, Turlapati SA, Handley C, Roux SJ, Kirti PB (2008) Ectopic expression of an annexin from Brassica juncea confers tolerance to abiotic and biotic stress treatments in transgenic tobacco. Plant Physiology and Biochemistry 46, 1019–1030.
| Ectopic expression of an annexin from Brassica juncea confers tolerance to abiotic and biotic stress treatments in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlGmurfF&md5=92438d6890c3c4ea7401ef0fa087e8fdCAS |
Jami SK, Dalal A, Divya K, Kirti PB (2009) Molecular cloning and characterization of five annexin genes from Indian mustard (Brassica juncea L. Czern and Coss). Plant Physiology and Biochemistry 47, 977–990.
| Molecular cloning and characterization of five annexin genes from Indian mustard (Brassica juncea L. Czern and Coss).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVajsrfL&md5=e3bbe4c2e11864a842dd67efae2a9292CAS |
Jami SK, Clark GB, Ayele BT, Ashe P, Kirti PB (2012a) Genome-wide comparative analysis of annexin superfamily in plants. PLoS One 7, e47801
| Genome-wide comparative analysis of annexin superfamily in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslWjtrnP&md5=feddc83a98f1340ed7e1d3f5448eae89CAS |
Jami SK, Clark GB, Ayele BT, Roux SJ, Kirti PB (2012b) Identification and characterization of annexin gene family in rice. Plant Cell Reports 31, 813–825.
| Identification and characterization of annexin gene family in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlsFelu7w%3D&md5=3268441ff94fa5a4ef4c1ea5a4565b9aCAS |
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8, 275–282.
Konopka-Postupolska D, Clark G, Goch G, Debski J, Floras K, Cantero A, Fijolek B, Roux S, Hennig J (2009) The role of annexin 1 in drought stress in Arabidopsis. Plant Physiology 150, 1394–1410.
| The role of annexin 1 in drought stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFerur4%3D&md5=a808b6846bf334ea0403a11e2b619435CAS |
Kovacs I, Ayaydin F, Oberschall A, Ipacs I, Bottka S, Pongor S, Dudits D, Toth E (1998) Immunolocalization of a novel annexin-like protein encoded by a stress and abscisic acid responsive gene in alfalfa. The Plant Journal 15, 185–197.
| Immunolocalization of a novel annexin-like protein encoded by a stress and abscisic acid responsive gene in alfalfa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlslWqtrY%3D&md5=f1b6946559fac097039c23a61ea90975CAS |
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsF2ltrzN&md5=b3423fc54b934bc23e6230ffb11da42fCAS |
Laohavisit A, Davies JM (2011) Annexins. New Phytologist 189, 40–53.
| Annexins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGhtQ%3D%3D&md5=041907e1cdcdaca6d861068f5cdc8796CAS |
Lee S, Lee EJ, Yang EJ, Lee JE, Park AR, Song WH, Park OK (2004) Proteomic identification of annexins, calcium-dependent membrane binding proteins that mediate osmotic stress and abscisic acid signal transduction in Arabidopsis. The Plant Cell 16, 1378–1391.
| Proteomic identification of annexins, calcium-dependent membrane binding proteins that mediate osmotic stress and abscisic acid signal transduction in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFWlsL4%3D&md5=8170be5ed573848bf352087bc41e9d26CAS |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods (San Diego, Calif.) 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=c6e730b8bcaab07d1e52bd2affd3622dCAS |
Lobell DB, Field CB (2007) Global scale climate–crop yield relationships and the impacts of recent warming. Environmental Research Letters 2, 014002
| Global scale climate–crop yield relationships and the impacts of recent warming.Crossref | GoogleScholarGoogle Scholar |
Loukehaich R, Wang T, Ouyang B, Ziaf K, Li H, Zhang J, Lu Y, Ye Z (2012) SpUSP, an annexin-interacting universal stress protein, enhances drought tolerance in tomato. Journal of Experimental Botany 63, 5593–5606.
| SpUSP, an annexin-interacting universal stress protein, enhances drought tolerance in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVSnu7fJ&md5=63ffeb296a0b1199909cb110d1ade118CAS |
Lu Y, Ouyang B, Zhang J, Wang T, Lu C, Han Q, Zhao S, Ye Z, Li H (2012) Genomic organization, phylogenetic comparison and expression profiles of annexin gene family in tomato (Solanum lycopersicum). Gene 499, 14–24.
| Genomic organization, phylogenetic comparison and expression profiles of annexin gene family in tomato (Solanum lycopersicum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkslWisbg%3D&md5=75a781311e7e4a92e29e0547da92ee91CAS |
Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, et al (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Research 45, D200–D203.
| CDD/SPARCLE: functional classification of proteins via subfamily domain architectures.Crossref | GoogleScholarGoogle Scholar |
Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, Battey NH, Davies JM (2008) Annexins: multifunctional components of growth and adaptation. Journal of Experimental Botany 59, 533–544.
| Annexins: multifunctional components of growth and adaptation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsValsro%3D&md5=edbbb962177c0e310f82db98c39e6acfCAS |
Moss SE, Morgan RO (2004) The annexins. Genome Biology 5, 219
| The annexins.Crossref | GoogleScholarGoogle Scholar |
Peng Z, Wang M, Li F, Lv H, Li C, Xia G (2009) A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Molecular & Cellular Proteomics 8, 2676–2686.
| A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOgs7fF&md5=a04f76d5abcd13237adb747f2aee1ed4CAS |
Qiao B, Zhang Q, Liu D, Wang H, Yin J, Wang R, He M, Cui M, Shang Z, Wang D, Zhu Z (2015) A calcium-binding protein, rice annexin OsANN1, enhances heat stress tolerance by modulating the production of H2O2. Journal of Experimental Botany 66, 5853–5866.
| A calcium-binding protein, rice annexin OsANN1, enhances heat stress tolerance by modulating the production of H2O2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVGju7zE&md5=6b60908a1ed152db57d1f03820c0d289CAS |
Ranty B, Aldon D, Galaud JP (2006) Plant calmodulins and calmodulin-related proteins: multifaceted relays to decode calcium signals. Plant Signaling & Behavior 1, 96–104.
| Plant calmodulins and calmodulin-related proteins: multifaceted relays to decode calcium signals.Crossref | GoogleScholarGoogle Scholar |
Rescher U, Gerke V (2004) Annexins – unique membrane binding proteins with diverse functions. Journal of Cell Science 117, 2631–2639.
| Annexins – unique membrane binding proteins with diverse functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFehtrs%3D&md5=c68f38e88b0fb44a37974de34c90270dCAS |
Rhee HJ, Kim GY, Huh JW, Kim SW, Na DS (2000) Annexin I is a stress protein induced by heat, oxidative stress and a sulfhydryl-reactive agent. European Journal of Biochemistry 267, 3220–3225.
| Annexin I is a stress protein induced by heat, oxidative stress and a sulfhydryl-reactive agent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvFymtrc%3D&md5=6b40464914e6401544d8ddd461c25cfaCAS |
Riewe D, Grosman L, Zauber H, Wucke C, Fernie AR, Geigenberger P (2008) Metabolic and developmental adaptations of growing potato tubers in response to specific manipulations of the adenylate energy status. Plant Physiology 146, 1579–1598.
| Metabolic and developmental adaptations of growing potato tubers in response to specific manipulations of the adenylate energy status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvVWju70%3D&md5=3ead01b68f4815eadb888131d788aa92CAS |
Rintala-Dempsey AC, Rezvanpour A, Shaw GS (2008) S100–annexin complexes – structural insights. The FEBS Journal 275, 4956–4966.
| S100–annexin complexes – structural insights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1OlsrjO&md5=a4ff8328b1c017aca7ca07612901e28dCAS |
Saitou N, Nei M (1987) The neighbor-joining method. A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
Serrago RA, Alzueta I, Savin R, Slafer GA (2013) Understanding grain yield responses to source–sink ratios during grain filling in wheat and barley under contrasting environments. Field Crops Research 150, 42–51.
| Understanding grain yield responses to source–sink ratios during grain filling in wheat and barley under contrasting environments.Crossref | GoogleScholarGoogle Scholar |
Tang W, He Y, Tu L, Wang M, Li Y, Ruan YL, Zhang X (2014) Down-regulating annexin gene GhAnn2 inhibits cotton fiber elongation and decreases Ca2+ influx at the cell apex. Plant Molecular Biology 85, 613–625.
| Down-regulating annexin gene GhAnn2 inhibits cotton fiber elongation and decreases Ca2+ influx at the cell apex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXptVeitLc%3D&md5=7f5472eb836d54cabbdcd844961049dfCAS |
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W, improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W, improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=c797f8c230df8ec8153a42ed609493b3CAS |
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant, Cell & Environment 25, 195–210.
| ABA-based chemical signalling: the co-ordination of responses to stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhslaktbY%3D&md5=518a1239ae8ed7907169bcc3283f5bedCAS |
Xu L, Tang Y, Gao S, Su S, Hong L, Wang W, Fang Z, Li X, Ma J, Quan W, Sun H, Li X, Wang Y, Liao X, Gao J, Zhang F, Li L, Zhao C (2016) Comprehensive analyses of the annexin gene family in wheat. BMC Genomics 17, 415
| Comprehensive analyses of the annexin gene family in wheat.Crossref | GoogleScholarGoogle Scholar |
Yamakawa H, Mitsuhara I, Ito N, Seo S, Kamada H, Ohashi Y (2001) Transcriptionally and post-transcriptionally regulated response of 13 calmodulin genes to tobacco mosaic virus-induced cell death and wounding in tobacco plant. European Journal of Biochemistry 268, 3916–3929.
| Transcriptionally and post-transcriptionally regulated response of 13 calmodulin genes to tobacco mosaic virus-induced cell death and wounding in tobacco plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVejsr4%3D&md5=43c943ef6f310c98d1bd42264b787ec2CAS |
Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteomic Structure Functional Biology 64, 643–651.
| Prediction of protein subcellular localization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt1OgtLo%3D&md5=9b705dbc677fe052b9038798d01ac000CAS |
Zhang F, Li S, Yang S, Wang L, Guo W (2015) Overexpression of a cotton annexin gene, GhAnn1, enhances drought and salt stress tolerance in transgenic cotton. Plant Molecular Biology 87, 47–67.
| Overexpression of a cotton annexin gene, GhAnn1, enhances drought and salt stress tolerance in transgenic cotton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsl2gsbnM&md5=5445f6c5c0464fb601a9605f4627904eCAS |
Zhou L, Duan J, Wang XM, Zhang HM, Duan MX, Liu JY (2011) Characterization of a novel annexin gene from cotton (Gossypium hirsutum cv CRI 35) and antioxidative role of its recombinant protein. Journal of Integrative Plant Biology 53, 347–357.
| Characterization of a novel annexin gene from cotton (Gossypium hirsutum cv CRI 35) and antioxidative role of its recombinant protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnslKnuro%3D&md5=e1b7dbd615fd1227ff097c616adfe743CAS |
Zhou ML, Yang XB, Zhang Q, Zhou M, Zhao EZ, Tang YX, Zhu XM, Shao JR, Wu YM (2013) Induction of annexin by heavy metals and jasmonic acid in Zea mays. Functional & Integrative Genomics 13, 241–251.
| Induction of annexin by heavy metals and jasmonic acid in Zea mays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXot1Gruro%3D&md5=40a400f8e79fb05c94f7dc60b0daccd5CAS |
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Current Opinion Plant Biology 6, 441–445.
| Regulation of ion homeostasis under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntVKhsbs%3D&md5=bf1aded61d8d247167eff1354b005b44CAS |
Zhu JK, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress in plants. Critical Reviews in Plant Sciences 16, 253–277.
| Molecular aspects of osmotic stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktlWntrw%3D&md5=fdf0685962ad7ab174a3f3ae4474378dCAS |
Zhu J, Yuan S, Wei G, Qian D, Wu X, Jia H, Gui M, Liu W, An L, Xiang Y (2014) Annexin5 is essential for pollen development in Arabidopsis. Molecular Plant 7, 751–754.
| Annexin5 is essential for pollen development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXls1Oiurc%3D&md5=f312910773bbe90f6ed74100d01369deCAS |
