Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

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 - https://doi.org/10.1071/FP17212
Submitted: 26 July 2017  Accepted: 12 November 2017   Published online: 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 |

Gerke V, Moss SE (2002) Annexins: from structure to function. Physiological Reviews 82, 331–371.
Annexins: from structure to function.CrossRef | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 1:CAS:528:DC%2BC28XhsF2ltrzN&md5=b3423fc54b934bc23e6230ffb11da42fCAS |

Laohavisit A, Davies JM (2011) Annexins. New Phytologist 189, 40–53.
Annexins.CrossRef | 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 | 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 | 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 |

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 | 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 | 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 |

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 | 1:CAS:528:DC%2BD1cXjsValsro%3D&md5=edbbb962177c0e310f82db98c39e6acfCAS |

Moss SE, Morgan RO (2004) The annexins. Genome Biology 5, 219
The annexins.CrossRef |

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 | 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 | 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 |

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 | 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 | 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 | 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 | 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 |

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 | 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 | 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 | 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 |

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 | 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 | 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 | 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 | 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 | 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 | 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 | 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 | 1:CAS:528:DC%2BC2cXls1Oiurc%3D&md5=f312910773bbe90f6ed74100d01369deCAS |



Supplementary MaterialSupplementary Material (733 KB) Export Citation