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In-depth proteome analysis reveals multiple pathways involved in tomato SlMPK1-mediated high-temperature responses

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Abstract

High temperature (HT) is one of the major environmental factors which limits plant growth and yield. The mitogen-activated protein kinase (MAPK) plays vital roles in environmental stress responses. However, the mechanisms triggered by MAPKs in plants in response to HT are still extremely limited. In this study, the proteomic data of differences between SlMPK1 RNA-interference mutant (SlMPK1i) and wild type and of tomato (Solanum lycopersicum) plants under HT stress using isobaric tags for relative and absolute quantitation (iTRAQ) was re-analyzed in depth. In total, 168 differently expressed proteins (DEPs) were identified in response to HT stress, including 38 DEPs only found in wild type, and 84 DEPs specifically observed in SlMPK1i after HT treatment. The majority of higher expression of 84 DEPs were annotated into photosynthesis, oxidation-reduction process, protein folding, translation, proteolysis, stress response, and amino acid biosynthetic process. More importantly, SlMPK1-mediated photosynthesis was confirmed by the physiological characterization of SlMPK1i with a higher level of photosynthetic capacity under HT stress. Overall, the results reveal a set of potential candidate proteins helping to further understand the intricate regulatory network regulated by SlMPK1 in response to HT.

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References

  • Ahammed GJ, Xu W, Liu A, Chen S (2018) COMT1 silencing aggravates heat stress-induced reduction in photosynthesis by decreasing chlorophyll content, photosystem II activity, and electron transport efficiency in tomato. Front Plant Sci 9

  • Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171:382–388

    Article  CAS  PubMed  Google Scholar 

  • Ballottari M, Mozzo M, Croce R, Morosinotto T, Bassi R (2009) Occupancy and functional architecture of the pigment binding sites of photosystem II antenna complex Lhcb5. J Biol Chem 284:8103–8113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bokszczanin KL, Fragkostefanakis S, Bostan H, Bovy A, Chaturvedi P, Chiusano ML, Li H (2013) Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front Plant Sci 4:315

    Article  PubMed  PubMed Central  Google Scholar 

  • Brauc S, De Vooght E, Claeys M, Geuns JMC, Höfte M, Angenon G (2012) Overexpression of arginase in Arabidopsis thaliana influences defence responses against Botrytis cinerea. Plant Biol 14:39–45

    Article  CAS  PubMed  Google Scholar 

  • Broin M, Cuiné S, Eymery F, Rey P (2002) The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell 14:1417–1432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bustin SA, Beaulieu JF, Huggett J, Jaggi R, Kibenge FS, Olsvik PA, Penning LC, Toegel S (2010) MIQE précis: practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments. BMC Mol Biol 11:74

    Article  PubMed  PubMed Central  Google Scholar 

  • Calatayud A, Barreno E (2004) Response to ozone in two lettuce varieties on chlorophyll a fluorescence, photosynthetic pigments and lipid peroxidation. Plant Physiol Biochem 42(6):549–555

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Thelen JJ (2010) The plastid isoform of triose phosphate isomerase is required for the post-germinative transition from heterotrophic to autotrophic growth in Arabidopsis. Plant Cell 22:77–90

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen W, Taylor NL, Chi Y, Millar AH, Lambers H, Finnegan PM (2014) The metabolic acclimation of Arabidopsis thaliana to arsenate is sensitized by the loss of mitochondrial LIPOAMIDE DEHYDROGENASE2, a key enzyme in oxidative metabolism. Plant Cell Environ 37:684–695

    Article  CAS  PubMed  Google Scholar 

  • Cho EJ, Yuen CY, Kang BH, Ondzighi CA, Staehelin LA, Christopher DA (2011) Protein disulfide isomerase-2 of Arabidopsis mediates protein folding and localizes to both the secretory pathway and nucleus, where it interacts with maternal effect embryo arrest factor. Mol Cells 32:459–475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding H, He J, Wu Y, Wu XX, Ge C, Wang Y, Xu W (2018) The tomato mitogen-activated protein kinase SlMPK1 is as a negative regulator of the high temperature stress response. Plant Physiol 177:633–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Echevarría-Zomeño S, Fernández-Calvino L, Castro-Sanz AB, López JA, Vázquez J, Castellano MM (2016) Dissecting the proteome dynamics of the early heat stress response leading to plant survival or death in Arabidopsis. Plant Cell Environ 39:1264–1278

    Article  PubMed  CAS  Google Scholar 

  • Evrard A, Kumar M, Lecourieux D, Lucks J, von Koskull-Döring P, Hirt H (2013) Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 1:e59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Foyer CH (2018) Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environ Exp Bot 154:134–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gawroński P, Witoń D, Vashutina K, Bederska M, Betliński B, Rusaczonek A, Karpiński S (2014) Mitogen-activated protein kinase 4 is a salicylic acid-independent regulator of growth but not of photosynthesis in Arabidopsis. Mol Plant 7:1151–1166

    Article  PubMed  CAS  Google Scholar 

  • Ge S, Jung D (2018) ShinyGO: a graphical enrichment tool for animals and plants. bioRxiv 315150

  • Guo Y, Wang Z, Guan X, Hu Z, Zhang Z, Zheng J, Lu Y (2017) Proteomic analysis of Potentilla fruticosa L. leaves by iTRAQ reveals responses to heat stress. PLoS One 1:e0182917

    Article  CAS  Google Scholar 

  • Hettenhausen C, Baldwin IT, Wu J (2012) Silencing MPK4 in Nicotiana attenuata enhances photosynthesis and seed production but compromises abscisic acid-induced stomatal closure and guard cell-mediated resistance to Pseudomonas syringae pv tomato DC3000. Plant Physiol 158:759–776

    Article  CAS  PubMed  Google Scholar 

  • Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43:103–111

    Article  CAS  PubMed  Google Scholar 

  • Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64:477–499

    Article  CAS  PubMed  Google Scholar 

  • Jia XY, Xu CY, Jing RL, Li RZ, Mao XG, Wang JP, Chang XP (2008) Molecular cloning and characterization of wheat calreticulin (CRT) gene involved in drought-stressed responses. J Exp Bot 59:739–751

    Article  CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    Article  CAS  PubMed  Google Scholar 

  • Keller M, Simm S (2018) The coupling of transcriptome and proteome adaptation during development and heat stress response of tomato pollen. BMC Genomics 19:447

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Keren N, Ohkawa H, Welsh EA, Liberton M, Pakrasi HB (2005) Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. Plant Cell 17:2768–2781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khozeai M, Fisk S, Lawson T, Gibon Y, Sulpice R, Stitt M, Raines CA (2015) Overexpression of plastid transketolase in tobacco results in a thiamine auxotrophic phenotype. Plant Cell 27:432–447

    Article  CAS  Google Scholar 

  • Kim EY, Seo YS, Lee H, Kim WT (2010) Constitutive expression of CaSRP1, a hot pepper small rubber particle protein homolog, resulted in fast growth and improved drought tolerance in transgenic Arabidopsis plants. Planta 232:71–83

    Article  CAS  PubMed  Google Scholar 

  • Kim EY, Park KY, Seo YS, Kim WT (2016) Arabidopsis small rubber particle protein homolog SRPs play dual roles as positive factors for tissue growth and development and in drought stress responses. Plant Physiol 170:2494–2510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kissen R, Winge P, Tran DHT, Jørstad TS, Størseth TR, Christensen T, Bones AM (2010) Transcriptional profiling of an Fd-GOGAT1/GLU1 mutant in Arabidopsis thaliana reveals a multiple stress response and extensive reprogramming of the transcriptome. BMC Genomics 11:190

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuo WY, Huang CH, Liu AC, Cheng CP, Li SH, Chang WC, Weiss C, Azem A, Jinn TL (2013) Chaperonin 20 mediates iron superoxide dismutase (FeSOD) activity independent of its co-chaperonin role in Arabidopsis chloroplasts. New Phytol 197:99–110

    Article  PubMed  CAS  Google Scholar 

  • Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529:84–87

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Cao Y, Zhang J, Chen S (2008) Characterization of Arabidopsis calreticulin mutants in response to calcium and salinity stresses. Prog Nat Sci 18:1219–1224

    Article  CAS  Google Scholar 

  • Li F, Wu QY, Sun YL, Wang LY, Yang XH, Meng QW (2010) Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses. Physiol Plant 139:421–434

    CAS  PubMed  Google Scholar 

  • Li Z, Yue H, Xing D (2012) MAP kinase 6-mediated activation of vacuolar processing enzyme modulates heat shock-induced programmed cell death in Arabidopsis. New Phytol 195:85–96

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Kabbage M, Liu W, Dickman MB (2016) Aspartyl protease mediated cleavage of AtBAG6 is necessary for autophagy and fungal resistance in plants. Plant Cell 28:233–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Last RL (2017) A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments. Proc Natl Acad Sci U S A 114:8110–8117

    Article  CAS  Google Scholar 

  • Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S (2007) Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51:941–954

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Beyer A, Aebersold R (2016) On the dependency of cellular protein levels on mRNA abundance. Cell 165:535–550

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Wang P, Zhang T, Li Y, Wang Y, Gao C (2018) Comprehensive analysis of BpHSP genes and their expression under heat stresses in Betula platyphylla. Environ Exp Bot 152:167–176

    Article  CAS  Google Scholar 

  • López-Martín MC, Becana M, Romero LC, Gotor C (2008) Knocking out cytosolic cysteine synthesis compromises the antioxidant capacity of the cytosol to maintain discrete concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol 147:562–572

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu Y, Hall DA, Last RL (2011) A small zinc finger thylakoid protein plays a role in maintenance of photosystem II in Arabidopsis thaliana. Plant Cell 23:1861–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marten H, Hyun T, Gomi K, Seo S, Hedrich R, Roelfsema MR (2008) Silencing of NtMPK4 impairs CO-induced stomatal closure, activation of anion channels and cytosolic Ca signals in Nicotiana tabacum guard cells. Plant J 55:698–708

    Article  CAS  PubMed  Google Scholar 

  • Mekonnen DW, Flügge UI, Ludewig F (2016) Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Sci 245:25–34

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signal. Annu Rev Phytopathol 51:245–266

    Article  CAS  PubMed  Google Scholar 

  • Miles GP, Samuel MA, Ranish JA, Donohoe SM, Sperrazzo GM, Ellis BE (2009) Quantitative proteomics identifies oxidant-induced, AtMPK6-dependent changes in Arabidopsis thaliana protein profiles. Plant Signal Behav 4:497–505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125

    Article  CAS  PubMed  Google Scholar 

  • Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signal. Trends Plant Sci 10:339–346

    Article  CAS  PubMed  Google Scholar 

  • Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22:53–65

    Article  CAS  PubMed  Google Scholar 

  • Parankusam S, Bhatnagar-Mathur P, Sharma KK (2017) Heat responsive proteome changes reveal molecular mechanisms underlying heat tolerance in chickpea. Environ Exp Bot 141:132–144

    Article  CAS  Google Scholar 

  • Park CJ, Seo YS (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31:323–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez DE, Hoyer JS, Johnson AI, Moody ZR, Lopez J, Kaplinsky NJ (2009) BOBBER1 is a noncanonical Arabidopsis small heat shock protein required for both development and thermotolerance. Plant Physiol 151:241–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pulido P, Llamas E, Rodriguez-Concepcion M (2017) Both Hsp70 chaperone and Clp protease plastidial systems are required for protection against oxidative stress. Plant Signal Behav 12:e1290039

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qiu Y, Xi J, Du L, Roje S, Poovaiah BW (2012) A dual regulatory role of Arabidopsis calreticulin-2 in plant innate immunity. Plant J 69:489–500

    Article  CAS  PubMed  Google Scholar 

  • Rayapuram N, Bigeard J, Alhoraibi H, Bonhomme L, Hesse AM, Vinh J, Pflieger D (2018) Quantitative phosphoproteomic analysis reveals shared and specific targets of Arabidopsis mitogen-activated protein kinases (MAPKs) MPK3, MPK4, and MPK6. Mol Cell Proteomics 17:61–80

    Article  CAS  PubMed  Google Scholar 

  • Reis PA, Rosado GL, Silva LA, Oliveira LC, Oliveira LB, Costa MD, Fontes EP (2011) The binding protein BiP attenuates stress-induced cell death in soybean via modulation of the N-rich protein-mediated signal pathway. Plant Physiol 157:1853–1865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero LC, Aroca MÁ, Laureano-Marín AM, Moreno I, García I, Gotor C (2014) Cysteine and cysteine-related signal pathways in Arabidopsis thaliana. Mol Plant 7:264–276

    Article  CAS  PubMed  Google Scholar 

  • Salvucci ME (2008) Association of Rubisco activase with chaperonin-60beta: a possible mechanism for protecting photosynthesis during heat stress. J Exp Bot 59:1923–1933

    Article  CAS  PubMed  Google Scholar 

  • Scranton MA, Yee A, Park SY, Walling LL (2012) Plant leucine aminopeptidases moonlight as molecular chaperones to alleviate stress-induced damage. J Biol Chem 287:18408–18417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seltmann MA, Stingl NE, Lautenschlaeger JK, Krischke M, Mueller MJ, Berger S (2010) Differential impact of lipoxygenase 2 and jasmonates on natural and stress-induced senescence in Arabidopsis. Plant Physiol 152:1940–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su PH, Li HM (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol 146:1231–1241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su J, Yang L, Zhu Q, Wu H, He Y, Liu Y, Xu J, Jiang D, Zhang S (2018) Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity. PLoS Biol 16:e2004122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signal in Arabidopsis. Mol Cell 15:141–152

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Huang B (2017) Lipid-and calcium-signaling regulation of HsfA2c-mediated heat tolerance in tall fescue. Environ Exp Bot 136:59–67

    Article  CAS  Google Scholar 

  • Wang M, Jiang W, Yu H (2010) Effects of exogenous epibrassinolide on photosynthetic characteristics in tomato (Lycopersicon esculentum Mill) seedlings under weak light stress. J Agric Food Chem 58:3642–3645

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Lan P, Gao H, Zheng L, Li W, Schmidt W (2013) Expression changes of ribosomal proteins in phosphate- and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics 14:783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zeng L, Xing D (2015) ROS-mediated enhanced transcription of CYP38 promotes the plant tolerance to high light stress by suppressing GTPase activation of PsbO2. Front Plant Sci 6:777

    PubMed  PubMed Central  Google Scholar 

  • Wu HY, Liu MS, Lin TP, Cheng YS (2011) Structural and functional assays of AtTLP18. 3 identify its novel acid phosphatase activity in thylakoid lumen. Plant Physiol 157:1015–1025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu H, Xu W, Xi H, Ma W, He Z, Ma M (2013) The ER luminal binding protein (BiP) alleviates Cd2+-induced programmed cell death through endoplasmic reticulum stress–cell death signal pathway in tobacco cells. J Plant Physiol 170:1434–1441

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Liu S, Takano T (2008) Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol Biol 68:131–143

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Wang P, Si T, Hsu CC, Wang L, Zayed O, Zhu JK (2017) MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Develop Cell 43:618–629

    Article  CAS  Google Scholar 

  • Zhou C, Cai Z, Guo Y, Gan S (2009) An Arabidopsis mitogen-activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol 150:167–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the China Postdoctoral Science Foundation funded project (20110491464, 2012T50520), National Natural Science Foundation of China (grant no. 31101092), and the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD).

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H.D. and C.G. conceived of the study. H.D. and Y.W. performed most of the experiment contents. G.Y. and X.W. analyzed part of the data. Other authors assisted in experiments. H.D. wrote the manuscript. C.G. guided the manuscript writing.

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Correspondence to Haidong Ding.

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Fig. S1

Putative amino acid metabolic processing pathway regulated by SlMPK1 suppression under high temperature (HT) stress. A putative amino acid metabolic processing pathway was constructed based on KEGG mapping. The red arrows represent up-regulated differentially expressed proteins (DEPs); the blue arrows indicate proteins identified as down-regulated DEPs. (PNG 1151 kb)

High resolution image (TIF 124 kb)

Fig. S2

Putative endoplasmic reticulum protein processing pathway regulated by SlMPK1 suppression under high temperature (HT) stress. A putative endoplasmic reticulum protein processing pathway was constructed based on KEGG mapping. The red arrows represent up-regulated differentially expressed proteins (DEPs). (PNG 1676 kb)

High resolution image (TIF 121 kb)

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Ding, H., Wu, Y., Yuan, G. et al. In-depth proteome analysis reveals multiple pathways involved in tomato SlMPK1-mediated high-temperature responses. Protoplasma 257, 43–59 (2020). https://doi.org/10.1007/s00709-019-01419-6

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