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Analysis of tomato plasma membrane H+-ATPase gene family suggests a mycorrhiza-mediated regulatory mechanism conserved in diverse plant species

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Abstract

In plants, the plasma membrane H+-ATPase (HA) is considered to play a crucial role in regulating plant growth and respoding to environment stresses. Multiple paralogous genes encoding different isozymes of HA have been identified and characterized in several model plants, while limited information of the HA gene family is available to date for tomato. Here, we describe the molecular and expression features of eight HA-encoding genes (SlHA1-8) from tomato. All these genes are interrupted by multiple introns with conserved positions. SlHA1, 2, and 4 were widely expressed in all tissues, while SlHA5, 6, and 7 were almost only expressed in flowers. SlHA8, the transcripts of which were barely detectable under normal or nutrient-/salt-stress growth conditions, was strongly activated in arbuscular mycorrhizal (AM) fungal-colonized roots. Extreme lack of SlHA8 expression in M161, a mutant defective to AM fungal colonization, provided genetic evidence towards the dependence of its expression on AM symbiosis. A 1521-bp SlHA8 promoter could direct the GUS reporter expression specifically in colonized cells of transgenic tobacco, soybean, and rice mycorrhizal roots. Promoter deletion assay revealed a 223-bp promoter fragment of SlHA8 containing a variant of AM-specific cis-element MYCS (vMYCS) sufficient to confer the AM-induced activity. Targeted deletion of this motif in the corresponding promoter region causes complete abolishment of GUS staining in mycorrhizal roots. Together, these results lend cogent evidence towards the evolutionary conservation of a potential regulatory mechanism mediating the activation of AM-responsive HA genes in diverse mycorrhizal plant species.

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References

  • Alsterfjord M, Sehnke PC, Arkell A, Larsson H, Svennelid F, Rosenquist M, Ferl RJ (2004) Plasma membrane H+-ATPase and 14-3-3 isoforms of Arabidopsis leaves: evidence for isoform specificity in the 14-3-3/H+-ATPase interaction. Plant Cell Physiol 45:1202–1210

    Article  CAS  PubMed  Google Scholar 

  • Arango M, GéVaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216:355–365

    CAS  PubMed  Google Scholar 

  • Balestrini R, Cosgrove DJ, Bonfante P (2005) Differential location of alpha-expansin proteins during the accommodation of root cells to an arbuscular mycorrhizal fungus. Planta 220:889–899

    Article  CAS  PubMed  Google Scholar 

  • Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132:618–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baxter IR, Young JC, Armstrong G, Foster N, Bogenschutz N, Cordova T, Peer WN, Hazen SP, Murphy AS, Harper JF (2005) A plasma membrane H+-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana. Proc Natl Acad Sci U S A 102:2649–2654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bitterlich M, Krügel U, Boldt-Burisch K, Franken P, Kühn C (2014) The sucrose transporter SlSUT2 from tomato interacts with brassinosteroid functioning and affects arbuscular mycorrhiza formation. Plant J 78:877–889

    Article  CAS  PubMed  Google Scholar 

  • Bobik K, Duby G, Nizet Y, Vandermeeren C, Stiernet P, Kanczewska J, Boutry M (2010) Two widely expressed plasma membrane H+-ATPase isoforms of Nicotiana tabacum are differentially regulated by phosphorylation of their penultimate threonine. Plant J 62:291–301

    Article  CAS  PubMed  Google Scholar 

  • Breuillin-Sessoms F, Floss DS, Gomez SK, Pumplin N, Ding Y, Levesque-Tremblay V, Noar RD, Daniels DA, Bravo A, Eaglesham JB, Benedito VA, Udvardi M, Harrison MJ (2015) Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell 27:1352–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang SJ, Puryear J, Cairney J (1994) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol 11:113–116

    Article  Google Scholar 

  • Chen AQ, Hu J, Sun SB, Xu GH (2007) Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol 173:817–831

    Article  CAS  PubMed  Google Scholar 

  • Chen AQ, Gu M, Sun SB, Zhu LL, Hong S, Xu GH (2011) Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytol 189:1157–1169

    Article  CAS  PubMed  Google Scholar 

  • Chen AQ, Chen X, Wang HM, Liao DH, Gu M, Qu HY, Sun SB, Xu GH (2014) Genome-wide investigation and expressionanalysis suggest diverse roles and geneticredundancy of Pht1 family genes in responseto Pi deficiency in tomato. BMC Plant Biol 14:61

    Article  PubMed  PubMed Central  Google Scholar 

  • David-Schwartz R, Badani H, Smadar W, Levy AA, Galili G, Kapulnik Y (2001) Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae. Plant J 27:561–569

    Article  CAS  PubMed  Google Scholar 

  • Duby G, Boutry M (2009) The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Eur J Physiol 457:645–655

    Article  CAS  Google Scholar 

  • Ewing NN, Bennett AB (1994) Assessment of the number and expression of P-Type H+-ATPase genes in tomato. Plant Physiol 106:547–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Favre P, Bapaume L, Bossolini E, Delorenzi M, Falquet L, Reinhardt D (2014) A novel bioinformatics pipeline to discover genes related to arbuscular mycorrhizal symbiosis based on their evolutionary conservation pattern among higher plants. BMC Plant Biol 14:333

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferrol N, Pozo MJ, Antelo M, Azcn-Aguilar C (2002) Arbuscular mycorrhizal symbiosis regulates plasma membrane H+-ATPase gene expression in tomato plants. J Exp Bot 53:1683–1687

    Article  CAS  PubMed  Google Scholar 

  • Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214

    Article  CAS  PubMed  Google Scholar 

  • Gévaudant F, Duby G, Ev S, Zhao RM, Morsomme P, Boutry M (2007) Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance. Plant Physiol 144:1763–1776

    Article  PubMed  PubMed Central  Google Scholar 

  • Gianinazzi-Pearson V, Arnould C, Oufattole M, Arango M, Gianinazzi S (2000) Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211:609–613

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Tolosano M, Volpe V, Kopriva S, Bonfante P (2014) Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol 204:609–619

    Article  CAS  PubMed  Google Scholar 

  • Glassop D, Smith S, Smith F (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698

    Article  CAS  PubMed  Google Scholar 

  • Guether M, Neuhäuser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo WB, Zhao J, Li XX, Qin L, Yan XL, Liao H (2011) A soybean β-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J 66:541–552

    Article  CAS  PubMed  Google Scholar 

  • Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617

    Article  CAS  PubMed  Google Scholar 

  • Haruta M, Sussman MR (2012) The effect of a genetically reduced plasma membrane proton motive force on vegetative growth of Arabidopsis. Plant Physiol 158:1158–1171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haruta M, Burch HL, Nelson RB, Barrett-Wilt G, Kline KG, Mohsin SB (2010) Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity. J Biol Chem 285:17918–17929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi Y, Takahashi K, Inoue S, Kinoshita T (2014) Abscisic acid suppresses hypocotyl elongation by dephosphorylating plasma membrane H+-ATPase in Arabidopsis thaliana. Plant Cell Physiol 55:845–853

    Article  CAS  PubMed  Google Scholar 

  • Herrera-Medina MJ, Steinkellner S, Vierheilig H, Bote JAO, Garrido JMG (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564

    Article  CAS  PubMed  Google Scholar 

  • Horsch RB, Fry JE, Homan NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231

    Article  CAS  Google Scholar 

  • Janicka-Russak M, Kobus G (2007) Modification of plasma membrane and vacuolar H+-ATPase in response to NaCl and ABA. J Plant Physiol 164:295–302

    Article  CAS  PubMed  Google Scholar 

  • Janicka-Russak M, Kabała K, Burzynski M (2012) Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. J Exp Bot 63:4133–4142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 104:1720–1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanczewska J, Marco S, Vandermeeren C, Maudoux O, Rigaud JL, Boutry M (2005) Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14-3-3 proteins converts a dimer into a hexamer. Proc Natl Acad Sci U S A 102:11675–11680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29

    Article  CAS  PubMed  Google Scholar 

  • Karandashov V, Nagy R, Wegmuller S, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 101:6285–6290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415

    Article  CAS  PubMed  Google Scholar 

  • Krajinski F, Hause B, Gianinazzi-Pearson V, Franken P (2002) MtHA1, a plasma membrane H+-ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol 4:754–761

    Article  CAS  Google Scholar 

  • Krajinski F, Courty PE, Sieh D, Franken P, Zhang HQ, Bucher M, Gerlach N, Kryvoruchko I, Zoeller D, Udvardi M, Hause B (2014) The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell 26:1808–1817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signaling and branching. Nature 483:341–344

    Article  CAS  PubMed  Google Scholar 

  • Lan P, Li WF, Lin WD, Santi S, Schmidt W (2013) Mapping gene activity of Arabidopsis root hairs. Genome Biol 14:R67

    Article  PubMed  PubMed Central  Google Scholar 

  • Lefebvre B, Arango M, Oufattole M, Crouzet J, Purnelle B, Boutry M (2005) Identification of a Nicotiana plumbaginifolia plasma membrane H+-ATPase gene expressed in the pollen tube. Plant Mol Biol 58:775–787

    Article  CAS  PubMed  Google Scholar 

  • Liao DH, Chen X, Chen AQ, Wang HM, Liu JJ, Liu JL, Gu M, Sun SB, Xu GH (2015) The characterization of six auxin-induced tomato GH3 genes uncovers a member, SlGH3.4, strongly responsive to arbuscular mycorrhizal symbiosis. Plant Cell Physiol 56:674–687

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol 7, e1000139

    Article  PubMed  PubMed Central  Google Scholar 

  • Lota F, Wegmüller S, Buer B, Sato S, Bräutigam A, Hanf B, Bucher M (2013) The cis-acting CTTC-P1BS module is indicative for gene function of LjVTI12., a Qb-SNARE protein gene that is required for arbuscule formation in Lotus japonicus. Plant J 74:280–293

    Article  CAS  PubMed  Google Scholar 

  • Maeda D, Ashida K, Iguchi K, Ashida K, Iguchi K, Chechetka SA, Hijikata A, Okusako Y, Deguchi Y, Izui K, Hata S (2006) Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol 47:807–817

    Article  CAS  PubMed  Google Scholar 

  • Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht MB, Xu GH, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42:236–250

    Article  CAS  PubMed  Google Scholar 

  • Okumura M, Inoue S, Takahashi K, Ishizaki K, Kohchi T, Kinoshita T (2012) Characterization of the plasma membrane H+-ATPase in the liverwort Marchantia polymorpha. Plant Physiol 159:826–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oufattole M, Arango M, Boutry M (2000) Identification and expression of three new Nicotiana plumbaginifolia genes which encode isoforms of a plasma membrane H+-ATPase, and one which is induced by mechanical stress. Planta 210:715–722

    Article  CAS  PubMed  Google Scholar 

  • Pumplin N, Harrison MJ (2009) Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 151:809–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson WR, Clark K, Young JC, Sussman MR (2004) An Arabidopsis thaliana plasma membrane proton pump is essential for pollen development. Genetics 168:1677–1687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosewarne GM, Smith FA, Schachtman DP, Smith SE (2007) Localization of proton-ATPase genes expressed in arbuscular mycorrhizal tomato plants. Mycorrhiza 17:249–258

    Article  CAS  PubMed  Google Scholar 

  • Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084

    Article  CAS  PubMed  Google Scholar 

  • Schaller A, Oecking C (1999) Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263–272

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shen H, Chen JH, Wang Z, Yang CY, Sasaki T, Yamamoto Y, Matsumoto H, Yan XL (2006) Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 57:1353–1362

    Article  CAS  PubMed  Google Scholar 

  • Sibole JV, Cabot C, Michalke W, Poschenrieder C, Barcelo J (2005) Relationship between expression of the PM H+-ATPase, growth and ion partitioning in the leaves of salt-treated Medicago species. Planta 221:557–566

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses growth or total P uptake. New Phytol 162:511–524

    Article  Google Scholar 

  • Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sperandioa MVL, Santosa LA, Buchera CA, Fernandesa MS, Souza SR (2011) Isoforms of plasma membrane H+-ATPase in rice root and shoot are differentially induced by starvation and resupply of NO3− or NH4+. Plant Sci 180:251–258

    Article  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d’un système radiculaire. Recherche de methods d’estimation ayant une signification fonctionelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221

    Google Scholar 

  • Upadhyaya NM, Surin B, Ramm K, Gaudron J, Schunmann PHD, Taylor W, Waterhouse PM, Wang MB (2000) Agrobacterium-mediated transformation of Australian rice cultivars Jarrah and Amaroo using modified promoters and selectable markers. Aust J Plant Physiol 27:201–210

    CAS  Google Scholar 

  • Wang ET, Yu N, Bano SA, Liu CW, Miller AJ, Cousins D, Zhang XW, Ratet P, Tadege M, Mysore KS, Downie JA, Murray JD, Oldroyd JED, Schultze M (2014) A H+-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell 26:1818–1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SY, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, Catausan S, Mattes N, Heuer S, Paszkowski U (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell 24:4236–4251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng HQ, Liu G, Kinoshita T, Zhang RP, Zhu YY, Shen QR, Xu GH (2012) Stimulation of phosphorus uptake by ammonium nutrition involves plasma membrane H+-ATPase in rice roots. Plant Soil 357:205–214

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (31372121, 31572188), the Fundamental Research Funds for the Central Universities (KYTZ201404), A Foundation for the Author of National Excellent Doctoral Dissertation of PR China (FANEDD, 201264), and the Program for New Century Excellent Talents in University (NCET-12-0860). We thank Professor Yoram Kapulnik from the Volcani Center of Israel for kindly providing us the seeds of M161 mutant and Professor Hong Liao from the South China Agricultural University for providing the Agrobacterium rhizogenes strain K599. We also thank Dr. Ajay Jain from National Research Centre on Plant Biotechnology, Pusa campus, New Delhi, India, for valuable comments and carefully correcting the manuscript.

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    1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China

      Junli Liu, Jianjian Liu, Aiqun Chen, Hongye Qu & Guohua Xu

    2. MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Nanjing Agricultural University, Nanjing, 210095, China

      Minjie Ji, Jiadong Chen, Xiaofeng Yang, Mian Gu & Guohua Xu

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    Junli Liu and Jianjian Liu contributed equally to this work.

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    Figure S1

    Chromosomal organization of the tomato HA genes. (DOC 633 kb)

    Figure S2

    Multiple alignment of deduced amino acid sequences of tomato HA genes. (DOC 289 kb)

    Figure S3

    Expression analysis of NtHA8 and NtPT4 in leaves and roots of tobacco mycorrhizal and non-mycorrhizal plants. (DOC 108 kb)

    Figure S4

    Histochemical staining of the mycorrhizal or non-mycorrhizal roots harboring different deletions of SlHA8 promoter fragments driving the GUS reporter gene. (DOC 680 kb)

    Table S1

    Identity matrix for the eight SlHA genes and their predicted amino acid sequences. (DOC 38 kb)

    Table S2

    Chromosomal localizations and molecular features of tomato HA genes. (DOC 25 kb)

    Table S3

    Gene-specific primers used for Real-time RT-PCR amplification of tomato HA genes. (DOC 19 kb)

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    Liu, J., Liu, J., Chen, A. et al. Analysis of tomato plasma membrane H+-ATPase gene family suggests a mycorrhiza-mediated regulatory mechanism conserved in diverse plant species. Mycorrhiza 26, 645–656 (2016). https://doi.org/10.1007/s00572-016-0700-9

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