Characterization of Banana SNARE Genes and Their Expression Analysis under Temperature Stress and Mutualistic and Pathogenic Fungal Colonization

SNAREs (soluble N-ethylmaleimide-sensitive-factor attachment protein receptors) are engines for almost all of the membrane fusion and exocytosis events in organism cells. In this study, we identified 84 SNARE genes from banana (Musa acuminata). Gene expression analysis revealed that the expression of MaSNAREs varied a lot in different banana organs. By analyzing their expression patterns under low temperature (4 °C), high temperature (45 °C), mutualistic fungus (Serendipita indica, Si) and fungal pathogen (Fusarium oxysporum f. sp. Cubense Tropical Race 4, FocTR4) treatments, many MaSNAREs were found to be stress responsive. For example, MaBET1d was up-regulate by both low and high temperature stresses; MaNPSN11a was up-regulated by low temperature but down-regulated by high temperature; and FocTR4 treatment up-regulated the expression of MaSYP121 but down-regulated MaVAMP72a and MaSNAP33a. Notably, the upregulation or downregulation effects of FocTR4 on the expression of some MaSNAREs could be alleviated by priorly colonized Si, suggesting that they play roles in the Si-enhanced banana wilt resistance. Foc resistance assays were performed in tobacco leaves transiently overexpressing MaSYP121, MaVAMP72a and MaSNAP33a. Results showed that transient overexpression of MaSYP121 and MaSNPA33a suppressed the penetration and spread of both Foc1 (Foc Race 1) and FocTR4 in tobacco leaves, suggesting that they play positive roles in resisting Foc infection. However, the transient overexpression of MaVAMP72a facilitated Foc infection. Our study can provide a basis for understanding the roles of MaSNAREs in the banana responses to temperature stress and mutualistic and pathogenic fungal colonization.

[1]  Xuefang Guan,et al.  The Single-Stranded DNA-Binding Gene Whirly (Why1) with a Strong Pathogen-Induced Promoter from Vitis pseudoreticulata Enhances Resistance to Phytophthora capsici , 2022, International journal of molecular sciences.

[2]  Changxin Luo,et al.  SNAREs Regulate Vesicle Trafficking During Root Growth and Development , 2022, Frontiers in Plant Science.

[3]  F. Liu,et al.  Influences of Serendipita indica and Dictyophorae echinovolvata on the Growth and Fusarium Wilt Disease Resistance of Banana , 2022, Biology.

[4]  Zonghua Wang,et al.  Genome-Wide Identification and Expression Analysis of SNARE Genes in Brassica napus , 2022, Plants.

[5]  Xueli Sun,et al.  Genome-wide identification of FAD gene family and their contributions to the temperature stresses and mutualistic and parasitic fungi colonization responses in banana. , 2022, International journal of biological macromolecules.

[6]  A. Drenth,et al.  The vulnerability of bananas to globally emerging disease threats. , 2021, Phytopathology.

[7]  W. Ji,et al.  Genome-wide identification, evolution, and expression of the SNARE gene family in wheat resistance to powdery mildew , 2021, PeerJ.

[8]  Margaret H. Frank,et al.  TBtools - an integrative toolkit developed for interactive analyses of big biological data. , 2020, Molecular plant.

[9]  Kunal Mukhopadhyay,et al.  Genome-Scale Identification, in Silico Characterization and Interaction Study Between Wheat SNARE and NPSN Gene Families Involved in Vesicular Transport , 2020, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[10]  F. Liu,et al.  Versatile Piriformospora indica and Its Potential Applications in Horticultural Crops , 2020 .

[11]  Rucha Karnik,et al.  Trafficking SNARE SYP132 Partakes in Auxin-Associated Root Growth1[OPEN] , 2020, Plant Physiology.

[12]  Xueli Sun,et al.  The root endophytic fungus Serendipita indica improves resistance of Banana to Fusarium oxysporum f. sp. cubense tropical race 4 , 2019, European Journal of Plant Pathology.

[13]  Xueli Sun,et al.  The root endophytic fungus Serendipita indica improves resistance of Banana to Fusarium oxysporum f. sp. cubense tropical race 4 , 2019, European Journal of Plant Pathology.

[14]  S. ruiz-Lara,et al.  Identification and transcriptional analysis of SNARE vesicle fusion regulators in tomato (Solanum lycopersicum) during plant development and a comparative analysis of the response to salt stress with wild relatives. , 2019, Journal of plant physiology.

[15]  J. Mercado-Blanco,et al.  Biological Control Agents Against Fusarium Wilt of Banana , 2019, Front. Microbiol..

[16]  Ji Huang,et al.  OsSYP121 Accumulates at Fungal Penetration Sites and Mediates Host Resistance to Rice Blast1 , 2019, Plant Physiology.

[17]  Jiang Lu,et al.  Molecular Characterization and Overexpression of VpRPW8s from Vitis pseudoreticulata Enhances Resistance to Phytophthora capsici in Nicotiana benthamiana , 2018, International journal of molecular sciences.

[18]  R. Visser,et al.  Functional Characterization of a Syntaxin Involved in Tomato (Solanum lycopersicum) Resistance against Powdery Mildew , 2017, Front. Plant Sci..

[19]  W. Hong,et al.  SNARE proteins in membrane trafficking , 2017, Traffic.

[20]  Ben Zhang,et al.  The Arabidopsis R-SNARE VAMP721 Interacts with KAT1 and KC1 K+ Channels to Moderate K+ Current at the Plasma Membrane[OPEN] , 2015, Plant Cell.

[21]  Erica E. Rosenbaum,et al.  The Gos28 SNARE Protein Mediates Intra-Golgi Transport of Rhodopsin and Is Required for Photoreceptor Survival* , 2014, The Journal of Biological Chemistry.

[22]  J. Mima,et al.  Multiple and distinct strategies of yeast SNAREs to confer the specificity of membrane fusion , 2014, Scientific Reports.

[23]  Saravanaraj N. Ayyampalayam,et al.  The banana (Musa acuminata) genome and the evolution of monocotyledonous plants , 2012, Nature.

[24]  Jinxing Lin,et al.  Arabidopsis R-SNARE Proteins VAMP721 and VAMP722 Are Required for Cell Plate Formation , 2011, PloS one.

[25]  Jun Yu,et al.  KaKs_Calculator 2.0: A Toolkit Incorporating Gamma-Series Methods and Sliding Window Strategies , 2010, Genom. Proteom. Bioinform..

[26]  D. Fasshauer,et al.  Differences in the SNARE evolution of fungi and metazoa. , 2009, Biochemical Society transactions.

[27]  V. Lipka,et al.  Arabidopsis non-host resistance to powdery mildews. , 2008, Current opinion in plant biology.

[28]  P. Schulze-Lefert,et al.  Secretory Pathways in Plant Immune Responses1 , 2008, Plant Physiology.

[29]  Adrian Hills,et al.  Functional Interaction of the SNARE Protein NtSyp 121 in Ca 2 1 Channel Gating , Ca 2 1 Transients and ABA Signalling of Stomatal Guard Cells , 2008 .

[30]  G. Jürgens,et al.  Co-option of a default secretory pathway for plant immune responses , 2008, Nature.

[31]  B. Haas,et al.  Insights into the Musa genome: Syntenic relationships to rice and between Musa species , 2008, BMC Genomics.

[32]  R. Panstruga,et al.  SNARE-ware: the role of SNARE-domain proteins in plant biology. , 2007, Annual review of cell and developmental biology.

[33]  K. Findlay,et al.  The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1 , 2007, Proceedings of the National Academy of Sciences.

[34]  H. Cai,et al.  Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. , 2007, Developmental cell.

[35]  A. Sanderfoot Increases in the Number of SNARE Genes Parallels the Rise of Multicellularity among the Green Plants1[W][OA] , 2007, Plant Physiology.

[36]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[37]  Heather Youngs,et al.  The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. , 2004, Molecular biology of the cell.

[38]  M. Blatt,et al.  A new catch in the SNARE. , 2004, Trends in plant science.

[39]  N. Raikhel,et al.  Traffic jams affect plant development and signal transduction , 2004, Nature Reviews Molecular Cell Biology.

[40]  Erich Kombrink,et al.  SNARE-protein-mediated disease resistance at the plant cell wall , 2003, Nature.

[41]  V. Page,et al.  The Expression of the t-SNARE AtSNAP33 Is Induced by Pathogens and Mechanical Stimulation1 , 2003, Plant Physiology.

[42]  M. Blatt,et al.  The abscisic acid-related SNARE homolog NtSyr1 contributes to secretion and growth: evidence from competition with its cytosolic domain. , 2002, The Plant cell.

[43]  Andrew A. Peden,et al.  A genomic perspective on membrane compartment organization , 2001, Nature.

[44]  R. J. Fisher,et al.  Control of fusion pore dynamics during exocytosis by Munc18. , 2001, Science.

[45]  N. Raikhel,et al.  The Arabidopsis genome. An abundance of soluble N-ethylmaleimide-sensitive factor adaptor protein receptors. , 2000, Plant physiology.

[46]  J. Rothman,et al.  Close Is Not Enough , 2000, The Journal of cell biology.

[47]  A. Brunger,et al.  Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  L. Staehelin The plant ER: a dynamic organelle composed of a large number of discrete functional domains. , 1997, The Plant journal : for cell and molecular biology.

[49]  W. Lukowitz,et al.  Cytokinesis in the Arabidopsis Embryo Involves the Syntaxin-Related KNOLLE Gene Product , 1996, Cell.

[50]  P. Schulze-Lefert,et al.  Identification of Genes Required for the Function of Non-Race-Specific mlo Resistance to Powdery Mildew in Barley. , 1996, The Plant cell.

[51]  R. Scheller,et al.  Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. , 1992, Science.

[52]  F E Bloom,et al.  The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations , 1989, The Journal of cell biology.

[53]  R. Scheller,et al.  VAMP-1: a synaptic vesicle-associated integral membrane protein. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[54]  T. Shiina,et al.  SYP71, a plant-specific Qc-SNARE protein, reveals dual localization to the plasma membrane and the endoplasmic reticulum in Arabidopsis. , 2008, Cell structure and function.

[55]  M. Newman,et al.  A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. , 2007, The Plant journal : for cell and molecular biology.