Abstract
Key message
The whole promoter regions of SUTs in Vitis were firstly isolated. SUTs are involved in the adaptation to biotic and abiotic stresses.
Abstract
The vulnerability of Vitis vinifera to abiotic and biotic stresses limits its yields. In contrast, Vitis amurensis displays resistance to environmental stresses, such as microbial pathogens, low temperatures, and drought. Sucrose transporters (SUTs) are important regulators for plant growth and stress tolerance; however, the role that SUTs play in stress resistance in V. amurensis is not known. Using V. amurensis Ruper. ‘Zuoshan-1’ and V. vinifera ‘Chardonnay’, we found that SUC27 was highly expressed in several vegetative organs of Zuoshan-1, SUC12 was weakly expressed or absent in most organs in both the species, and the distribution of SUC11 in source and sink organs was highest in Zuoshan-1. A search for cis-regulatory elements in the promoter sequences of SUTs revealed that they were regulated by light, environmental stresses, physiological correlation, and hormones. The SUTs in Zuoshan-1 mostly show a higher and rapid response than in Chardonnay under the induction by Plasmopara viticola infection, cold, water deficit, and dark conditions. The induction of SUTs was associated with the upregulation of key genes involved in sucrose metabolism and the biosynthesis of plant hormones. These results indicate that stress resistance in Zuoshan-1 is governed by the differential distribution and induction of SUTs by various stimuli, and the subsequent promotion of sucrose metabolism and hormone synthesis.
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References
Afoufa-Bastien D, Medici A, Jeauffre J, Coutos-Thevenot P, Lemoine R, Atanassova R, Laloi M (2010a) The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling. BMC Plant Biol 10:1741–1763. https://doi.org/10.1186/1471-2229-10-245
Afoufa-Bastien D, Medici A, Jeauffre J, Coutos-Thevenot P, Lemoine R, Atanassova R, Laloi M (2010b) The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling. BMC Plant Biol 10:245. https://doi.org/10.1186/1471-2229-10-245
Ageorges A, Issaly R, Picaud S, Delrot S, Romieu C (2000) Identification and functional expression in yeast of a grape berry sucrose carrier. Plant Physiol Biochem 38:177–185
Albertazzi G et al (2009) Gene expression in grapevine cultivars in response to Bois Noir phytoplasma infection. Plant Sci 176:792–804. https://doi.org/10.1016/j.plantsci.2009.03.001
Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488. https://doi.org/10.1007/s11103-008-9435-0
Barker L et al (2000) SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12:1153–1164
Baroja-Fernandez E et al (2012) Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production. Proc Natl Acad Sci USA 109:321–326. https://doi.org/10.1073/pnas.1117099109
Beale MH, Ward JL (1998) Jasmonates: key players in the plant defence. Nat Prod Rep 15:533–548
Beck EH, Fettig S, Knake C, Hartig K, Bhattarai T (2007) Specific and unspecific responses of plants to cold and drought stress. J Biosci 32:501–510
Bieniawska Z et al (2007) Analysis of the sucrose synthase gene family in Arabidopsis. Plant J 49:810–828. https://doi.org/10.1111/j.1365-313X.2006.03011.x
Cai Y, Tu W, Zu Y, Jing Y, Xu Z, Lu J, Zhang Y (2017) Overexpression of a grapevine sucrose transporter (VvSUC27) in tobacco improves plant growth rate in the presence of sucrose in vitro. Front Plant Sci 8:1069. https://doi.org/10.3389/fpls.2017.01069
Calonje M, Cubas P, Martinez-Zapater JM, Carmona MJ (2004) Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiol 135:1491–1501. https://doi.org/10.1104/pp.104.040832
Chincinska IA, Liesche J, Krugel U, Michalska J, Geigenberger P, Grimm B, Kuhn C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146:515–528. https://doi.org/10.1104/pp.107.112334
Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381. https://doi.org/10.1146/annurev.arplant.48.1.355
Davies C, Robinson SP (1996) Sugar accumulation in grape berries. Cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues. Plant Physiol 111:275–283
Davies C, Wolf T, Robinson SP (1999) Three putative sucrose transporters are differentially expressed in grapevine tissues. Plant Sci 147:93–100. https://doi.org/10.1016/S0168-9452(99)00059-X
de Torres-Zabala M et al (2007) Pseudomonas syringae pv. Tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. Embo J 26:1434–1443. https://doi.org/10.1038/sj.emboj.7601575
Deeken R, Ache P, Kajahn I, Klinkenberg J, Bringmann G, Hedrich R (2008) Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. Plant J 55:746–759. https://doi.org/10.1111/j.1365-313X.2008.03555.x
Deluc LG et al (2007) Transcriptomic and metabolite analyses of Cabernet sauvignon grape berry development. BMC Genom 8:429. https://doi.org/10.1186/1471-2164-8-429
Diaz-Riquelme J, Martinez-Zapater JM, Carmona MJ (2014) Transcriptional analysis of tendril and inflorescence development in grapevine (Vitis vinifera L.). PloS ONE 9:e92339. https://doi.org/10.1371/journal.pone.0092339
Figueiredo A, Monteiro F, Fortes AM, Bonow-Rex M, Zyprian E, Sousa L, Pais MS (2012) Cultivar-specific kinetics of gene induction during downy mildew early infection in grapevine. Funct Integr Genom 12:379–386. https://doi.org/10.1007/s10142-012-0261-8
Forcat S, Bennett MH, Mansfield JW, Grant MR (2008) A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods 4:16. https://doi.org/10.1186/1746-4811-4-16
Frost CJ, Nyamdari B, Tsai CJ, Harding SA (2012) The tonoplast-localized sucrose transporter in populus (PtaSUT4) regulates whole-plant water relations, responses to water stress, and photosynthesis. PloS ONE 7:e44467. https://doi.org/10.1371/journal.pone.0044467
Gamm M et al (2011) Changes in carbohydrate metabolism in Plasmopara viticola–infected grapevine leaves. Mol Plant Microbe Interact 24:1061–1073. https://doi.org/10.1094/Mpmi-02-11-0040
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
Gong X et al (2015) Arabidopsis AtSUC2 and AtSUC4, encoding sucrose transporters, are required for abiotic stress tolerance in an ABA-dependent pathway. Physiol Plant 153:119–136. https://doi.org/10.1111/ppl.12225
Guerreiro A, Figueiredo J, Silva MS, Figueiredo A (2016) Linking jasmonic acid to grapevine resistance against the biotrophic oomycete Plasmopara viticola. Front Plant Sci 7:565. https://doi.org/10.3389/Fpls.2016.00565
Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776
Hamiduzzaman MM, Jakab G, Barnavon L, Neuhaus JM, Mauch-Mani B (2005) Beta-aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Mol Plant Microbe Interact 18:819–829. https://doi.org/10.1094/MPMI-18-0819
Hayat S, Irfan M, Wani AS, Alyemeni MN, Ahmad A (2012) Salicylic acids: local systemic or inter-systemic regulators? Plant Signal Behav 7:93–102. https://doi.org/10.4161/psb.7.1.18620
Hayes MA, Feechan A, Dry IB (2010) Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal. Infect Plant Physiol 153:211–221. https://doi.org/10.1104/pp.110.154765
Hren M et al (2009) ‘Bois noir’ phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine. BMC Genom 10:460. https://doi.org/10.1186/1471-2164-10-460
Imlau A, Truernit E, Sauer N (1999) Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309–322
Ivashikina N, Deeken R, Ache P, Kranz E, Pommerrenig B, Sauer N, Hedrich R (2003) Isolation of AtSUC2 promoter-GFP-marked companion cells for patch-clamp studies and expression profiling. Plant J 36:931–945. https://doi.org/10.1046/j.1365-313X.2003.01931.x
Jia W et al (2015) Accumulation sucrose transporter atsuc9 mediated by a low sucrose level is involved in Arabidopsis abiotic stress resistance by regulating sucrose distribution and ABA. Plant Cell Physiol 56:1574–1587. https://doi.org/10.1093/pcp/pcv082
Julius BT, Leach KA, Tran TM, Mertz RA, Braun DM (2017) Sugar transporters in plants: new insights and discoveries. Plant Cell physiol 58:1442–1460. https://doi.org/10.1093/pcp/pcx090
Koster KL (1991) Glass-formation and desiccation tolerance. Seeds Plant Physiol 96:302–304. https://doi.org/10.1104/Pp.96.1.302
Lalonde S, Boles E, Hellmann H, Barker L, Patrick JW, Frommer WB, Ward JM (1999) The dual function of sugar carriers transport sugar sensing. Plant Cell 11:707–726
Lepka P, Stitt M, Moll E, Seemuller E (1999) Effect of phytoplasmal infection on concentration and translocation of carbohydrates and amino acids in periwinkle and tobacco. Physiol Mol Plant 55:59–68. https://doi.org/10.1006/pmpp.1999.0202
Liu LY, Li H (2013) Review: research progress in amur grape, Vitis amurensis Rupr. Can J Plant Sci 93:565–575. https://doi.org/10.4141/Cjps2012-202
Liu SL, Wu J, Zhang P, Hasi G, Huang Y, Lu J, Zhang YL (2016) Response of phytohormones and correlation of SAR signal pathway genes to the different resistance levels of grapevine against Plasmopara viticola infection. Plant Physiol Biochem 107:56–66. https://doi.org/10.1016/j.plaphy.2016.05.020
Ma YY, Zhang YL, Shao H, Lu J (2009) Differential physio-biochemical responses to cold stress of cold-tolerant and non-tolerant grapes (Vitis L.) from China. J Agron Crop Sci 196:212–219. https://doi.org/10.1111/j.1439-037X.2009.00405.x
Ma YY, Zhang YL, Shao H, Lu J (2010) Differential physio-biochemical responses to cold stress of cold-tolerant and non-tolerant grapes (Vitis L.) from China. J Agron Crop Sci 196:212–219. https://doi.org/10.1111/j.1439-037X.2009.00405.x
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158. https://doi.org/10.1016/j.abb.2005.10.018
Manning K, Davies C, Bowen HC, White PJ (2001) Functional characterization of two ripening-related sucrose transporters from grape berries. Ann Bot Lond 87:125–129. https://doi.org/10.1006/anbo.2000.1316
Maust BE, Espadas F, Talavera C, Aguilar M, Santamaria JM, Oropeza C (2003) Changes in carbohydrate metabolism in coconut palms infected with the lethal yellowing. Phytoplasma Phytopathol 93:976–981. https://doi.org/10.1094/Phyto.2003.93.8.976
Meyer S, Lauterbach C, Niedermeier M, Barth I, Sjolund RD, Sauer N (2004) Wounding enhances expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues. Plant Physiol 134:684–693. https://doi.org/10.1104/pp.103.033399
Moreno D, Berli FJ, Piccoli PN, Bottini R (2011) Gibberellins and abscisic acid promote carbon allocation in roots and berries of grapevines. J Plant Growth Regul 30:220–228. https://doi.org/10.1007/s00344-010-9186-4
Morgan JM (1984) Osmoregulation and water-stress in higher-plants. Ann Rev Plant Physiol Plant Mol Biol 35:299–319. https://doi.org/10.1146/annurev.pp.35.060184.001503
Murcia G et al (2016) ABA and GA(3) increase carbon allocation in different organs of grapevine plants by inducing accumulation of non-structural carbohydrates in leaves, enhancement of phloem area and expression of sugar transporters. Physiol Plant 156:323–337. https://doi.org/10.1111/ppl.12390
Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5:986–992. https://doi.org/10.1038/nprot.2010.37
Pastenes C, Villalobos L, Rios N, Reyes F, Turgeon R, Franck N (2014) Carbon partitioning to berries in water stressed grapevines: the role of active transport in leaves and fruits. Environ Exp Bot 107:154–166. https://doi.org/10.1016/j.envexpbot.2014.06.009
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295. https://doi.org/10.1016/j.pbi.2011.02.001
Perazzolli M et al (2012) Downy mildew resistance induced by Trichoderma harzianum T39 in susceptible grapevines partially mimics transcriptional changes of resistant genotypes BMC Genom 13:660. https://doi.org/10.1186/1471-2164-13-660
Rabbani MA et al (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767. https://doi.org/10.1104/pp.103.025742
Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2:198–206. https://doi.org/10.1016/S1369-5266(99)80036-3
Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3:942–955. https://doi.org/10.1093/mp/ssq044
Santi S, Grisan S, Pierasco A, De Marco F, Musetti R (2013) Laser microdissection of grapevine leaf phloem infected by stolbur reveals site-specific gene responses associated to sucrose transport and metabolism. Plant Cell Environ 36:343–355. https://doi.org/10.1111/j.1365-3040.2012.02577.x
Schulze W, Weise A, Frommer WB, Ward JM (2000) Function of the cytosolic N-terminus of sucrose transporter AtSUT2 in substrate affinity. FEBS Lett 485:189–194
Seo HS et al (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98:4788–4793. https://doi.org/10.1073/pnas.081557298
Somani BL, Khanade J, Sinha R (1987) A modified anthrone-sulfuric acid method for the determination of fructose in the presence of certain proteins. Anal Biochem 167:327–330
Tian Y, Zhang H, Pan X, Chen X, Zhang Z, Lu X, Huang R (2011) Overexpression of ethylene response factor TERF2 confers cold tolerance in rice seedlings. Transgenic Res 20:857–866. https://doi.org/10.1007/s11248-010-9463-9
Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86. https://doi.org/10.1186/s12870-016-0771-y
Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plant 127:167–181. https://doi.org/10.1111/j.1399-3054.2006.00672.x
Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525. https://doi.org/10.1111/j.1365-3040.2009.02052.x
Wu JA, Zhang YL, Zhang HQ, Huang H, Folta KM, Lu JA (2010) Whole genome wide expression profiles of Vitis amurensis grape responding to downy mildew by using Solexa sequencing technology. BMC Plant Biol 10:234. https://doi.org/10.1186/1471-2229-10-234
Xu QY, Chen SY, Ren YJ, Chen SL, Liesche J (2018) Regulation of sucrose transporters and phloem loading in response to environmental cues. Plant Physiol 176:930–945. https://doi.org/10.1104/pp.17.01088
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. https://doi.org/10.1146/annurev.arplant.57.032905.105444
Yu SM (1999) Cellular and genetic responses of plants to sugar starvation. Plant Physiol 121:687–693
Zhang YL, Meng QY, Zhu HL, Guo Y, Gao HY, Luo YB, Lu JA (2008) Functional characterization of a LAHC sucrose transporter isolated from grape berries in yeast. Plant Growth Regul 54:71–79. https://doi.org/10.1007/s10725-007-9226-7
Zhang SW, Gan YT, Xu BL (2016) Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front Plant Sci 7:1405. https://doi.org/10.3389/Fpls.2016.01405
Zhu Z et al (2013) Three ERF transcription factors from Chinese wild grapevine Vitis pseudoreticulata participate in different biotic and abiotic stress-responsive pathways. J Plant Physiol 170:923–933. https://doi.org/10.1016/j.jplph.2013.01.017
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This work was supported by the National Natural Science Foundation of China (Grant No. 30900969).
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YLZ, YMC, and JL designed the research. YMC, JY, QKL, ZFD and SLL performed the research. YMC and YLZ drafted the article.
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Cai, Y., Yan, J., Li, Q. et al. Sucrose transporters of resistant grapevine are involved in stress resistance. Plant Mol Biol 100, 111–132 (2019). https://doi.org/10.1007/s11103-019-00847-5
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DOI: https://doi.org/10.1007/s11103-019-00847-5