Physiological and transcriptomic analysis of tomato in response to sub-optimal temperature stress

References

• Heidarvand L, Millar AH, Taylor NL. Responses of the mitochondrial respiratory system to low temperature in plants. Crit Rev Plant Sci. 2017;36(4):217–11. doi:10.1080/07352689.2017.1375836.
   Web of Science ®Google Scholar
• Meng SD, Xiang HZ, Yang XR, Ye YZ, Han LL, Xu T, Liu YF, Wang F, Tan CH, Qi MF, et al. Effects of low temperature on pedicel abscission and auxin synthesis key genes of tomato. Int J Mol Sci. 2023;24(11):9186. doi:10.3390/ijms24119186.
   PubMed Web of Science ®Google Scholar
• Camejo D, Rodríguez P, Morales A, Dell’amico JM, Torrecillas A, Alarcón JJ. High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J Plant Physiol. 2005;162(3):281–289. doi:10.1016/j.jplph.2004.07.014.
   PubMed Web of Science ®Google Scholar
• Criddle RS, Smith BN, Hansen LD. A respiration based description of plant growth rate responses to temperature. Planta. 1997;201(4):441–445. doi:10.1007/s004250050087.
   Web of Science ®Google Scholar
• Miao Y, Ren J, Zhang YZY, Chen X, Qi M, Li T, Zhang G, Liu Y. Effect of low root-zone temperature on photosynthesis, root structure and mineral element absorption of tomato seedlings. Sci Hortic (Amsterdam). 2023;315:111956. doi:10.1016/j.scienta.2023.111956.
   Web of Science ®Google Scholar
• Ntatsi G, Savvas D, Druege U, Schwarz D. Contribution of phytohormones in alleviating the impact of sub-optimal temperature stress on grafted tomato. Sci Hortic (Amsterdam). 2013;149:28–38. doi:10.1016/j.scienta.2012.09.002.
   Web of Science ®Google Scholar
• Ntatsi G, Savvas D, Papasotiropoulos V, Katsileros A, Zrenner RM, Hincha DK, Zuther E, Schwarz D. Rootstock sub-optimal temperature tolerance determines transcriptomic responses after long-term root cooling in rootstocks and scions of grafted tomato plants. Front Plant Sci. 2017;8:911. doi:10.3389/fpls.2017.00911.
   PubMed Web of Science ®Google Scholar
• Schwarz D, Rouphael Y, Colla G, Venema JH. Grafting as a tool to improve tolerance of vegetables to abiotic stresses: thermal stress, water stress and organic pollutants. Sci Hortic (Amsterdam). 2010;127(2):162–171. doi:10.1016/j.scienta.2010.09.016.
   Web of Science ®Google Scholar
• Li YT, Zhang J, Wang SJ, Zhang HE, Liu YC, Yang MS. Integrative transcriptomic and metabolomic analyses reveal the flavonoid biosynthesis of Pyrus hopeiensis flowers under cold stress. Hortic Plant J. 2023;9(3):395–413. doi:10.1016/j.hpj.2022.11.004.
   Web of Science ®Google Scholar
• Zhao Y, Zhou M, Xu K, Li JH, Li SS, Zhang SH, Yang XJ. Integrated transcriptomics and metabolomics analyses provide insights into cold stress response in wheat. Crop J. 2019;7(6):857–866. doi:10.1016/j.cj.2019.09.002.
   Google Scholar
• Hou W, Sun AH, Yang FS, Zhan YF, Li SZ, Zhou ZD. Effects of sub-optimal temperatures and low light intensity on growth and anti-oxidant enzyme activities in watermelon (Citrullus lanatus) seedlings. J Hortic Sci Biotech. 2015;90(1):92–98. doi:10.1080/14620316.2015.11513158.
   Web of Science ®Google Scholar
• Venema JH, Posthumus F, van Hasselt PR. Impact of suboptimal temperature on growth, photosynthesis, leaf pigments and carbohydrates of domestic and high-altitude wild lycopersicon species. J Plant Pathol. 1999;155(6):711–718. doi:10.1016/S0176-1617(99)80087-X.
   Google Scholar
• Ploschuk EL, Bado LA, Salinas M, Wassner DF, Windauer LB, Insausti P. Photosynthesis and fluorescence responses of jatropha curcas to chilling and freezing stress during early vegetative stages. Environ Exp Bot. 2014;102:18–26. doi:10.1016/j.envexpbot.2014.02.005.
   Web of Science ®Google Scholar
• Allen DJ, Ort DR. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci. 2001;6(1):36–42. doi:10.1016/S1360-1385(00)01808-2.
   PubMed Web of Science ®Google Scholar
• Cao X, Jiang FL, Wang X, Zang YW, Wu Z. Comprehensive evaluation and screening for chilling-tolerance in tomato lines at the seedling stage. Euphytica. 2015;205(2):569–584. doi:10.1007/s10681-015-1433-0.
   Web of Science ®Google Scholar
• Ronga D, Rizza F, Badeck FW, Milc J, Laviano L, Montevecchi G, Pecchioni N, Francia E. Physiological responses to chilling in cultivars of processing tomato released and cultivated over the past decades in Southern Europe. Sci Hortic (Amsterdam). 2018;231:118–125. doi:10.1016/j.scienta.2017.12.033.
   Web of Science ®Google Scholar
• Masalo I, Oca J. Evaluation of a portable chlorophyll optical meter to estimate chlorophyll concentration in the green seaweedUlva ohnoi. J Appl Phycol. 2020;32(6):4171–4174. doi:10.1007/s10811-020-02257-3.
   Web of Science ®Google Scholar
• Mizoguchi T, Harada J, Tamiaki H. Characterization of chlorophyll pigments in the mutant lacking 8-vinyl reductase of green photosynthetic bacterium chlorobaculum tepidum. Bioorgan med chem. 2012;20(23):6803–6810. doi:10.1016/j.bmc.2012.09.054.
   PubMed Web of Science ®Google Scholar
• Gerganova M, Stanoeva D, Popova A, Velitchkova M. Pigment content and oxygen evolution of tomato plants as affected by long term treatment at suboptimal temperature. Cr Acad Bulg Sci. 2016;69:1429–1436.
   Google Scholar
• Baker NR, Rosenqvist E. Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot. 2004;55(403):1607–1621. doi:10.1093/jxb/erh196.
   PubMed Web of Science ®Google Scholar
• Zhou R, Yu XQ, Ottosen CO, Rosenqvist E, Zhao LP, Wang YL, Yu WG, Zhao TM, Wu Z. Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol. 2017;17(1):24. doi:10.1186/s12870-017-0974-x.
   PubMedGoogle Scholar
• Zhou R, Wu Z, Wang X, Rosenqvist E, Wang YL, Zhao TM, Ottosen CO. Evaluation of temperature stress tolerance in cultivated and wild tomatoes using photosynthesis and chlorophyll fluorescence. Hortic Environ Biote. 2018;59(4):499–509. doi:10.1007/s13580-018-0050-y.
   Web of Science ®Google Scholar
• Zhou X, Ge ZM, Kellomaki S, Wang KY, Peltola H, Martikainen P. Effects of elevated CO2 and temperature on leaf characteristics, photosynthesis and carbon storage in aboveground biomass of a boreal bioenergy crop (phalaris arundinacea L.) under varying water regimes. GCB Bioenergy. 2011;3(3):223–234. doi:10.1111/j.1757-1707.2010.01075.x.
   Google Scholar
• Zhu J, Zhang KX, Wang WS, Gong W, Liu WC, Chen HG, Xu HH, Lu YT. Low temperature inhibits root growth by reducing auxin accumulation via ARR1/12. Plant Cell Physiol. 2015;56(4):727–736. doi:10.1093/pcp/pcu217.
   PubMed Web of Science ®Google Scholar
• Farrar JF, Jones DL. The control of carbon acquisition by roots. New Phytol. 2008;147(1):43–53. doi:10.1046/j.1469-8137.2000.00688.x.
   Google Scholar
• Nagel KA, Kastenholz B, Jahnke S, Van Dusschoten D, Aach T, Muhlich M, Truhn D, Scharr H, Terjung S, Walter A, et al. Temperature responses of roots: impact on growth, root system architecture and implications for phenotyping. Funct Plant Biol. 2009;36(10–11):947–959. doi:10.1071/FP09184.
   PubMed Web of Science ®Google Scholar
• Iseri OD, Korpe DA, Sahin FI, Haberal M. Hydrogen peroxide pretreatment of roots enhanced oxidative stress response of tomato under cold stress. Acta Physiol Plant. 2013;35(6):1905–1913. doi:10.1007/s11738-013-1228-7.
   Web of Science ®Google Scholar
• Zhang ZD, Zhang YH, Yuan LQ, Zhou F, Gao Y, Kang Z, Li TL, Hu XH. Exogenous 5-aminolevulinic acid alleviates low-temperature injury by regulating glutathione metabolism and ss-alanine metabolism in tomato seedling roots. Ecotox Environ Safe. 2022b;245:114112. doi:10.1016/j.ecoenv.2022.114112.
   PubMed Web of Science ®Google Scholar
• Milc J, Bagnaresi P, Aragona M, Valente MT, Biselli C, Infantino A, Francia E, Pecchioni N. Comparative transcriptome profiling of the response to Pyrenochaeta lycopersici in resistant tomato cultivar mogeor and its background genotype-susceptible moneymaker. Funct Integr Genomic. 2019;19(5):811–826. doi:10.1007/s10142-019-00685-0.
   PubMed Web of Science ®Google Scholar
• Su LH, Xie YD, He ZQ, Zhang JW, Tang Y, Zhou XT. Network response of two cherry tomato (lycopersicon esculentum) cultivars to cadmium stress as revealed by transcriptome analysis. Ecotox Environ Safe. 2021;222:112473. doi:10.1016/j.ecoenv.2021.112473.
   PubMed Web of Science ®Google Scholar
• Gao H, Yang WJ, Li CX, Zhou XG, Gao DM, Rahman MKU, Li NH, Wu FZ. Gene expression and K+ uptake of two tomato cultivars in response to sub-optimal temperature. Plants-Basel. 2020;9(1):20. doi:10.3390/plants9010065.
   Web of Science ®Google Scholar
• Arnon DI. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in beta vulgaris. Plant Physiol. 1949;24(1):1. doi:10.1104/pp.24.1.1.
   PubMed Web of Science ®Google Scholar
• Zhang H, Hu H, Zhang XB, Wang KL, Song TQ, Zeng FP. Detecting suaeda salsa L. chlorophyll fluorescence response to salinity stress by using hyperspectral reflectance. Acta Physiol Plant. 2012;34(2):581–588. doi:10.1007/s11738-011-0857-y.
   Web of Science ®Google Scholar
• Huang ZA, Jiang DA, Yang Y, Sun JW, Jin SH. Effects of nitrogen deficiency on gas exchange, chlorophyll fluorescence, and antioxidant enzymes in leaves of rice plants. Photosynthetica. 2004;42(3):357–364. doi:10.1023/B:PHOT.0000046153.08935.4c.
   Web of Science ®Google Scholar
• Shi HT, Qian YQ, Tan DX, Reiter RJ, He CZ. Melatonin induces the transcripts of CBF/DREB1s and their involvement in both abiotic and biotic stresses in arabidopsis. J Pineal Res. 2015;59(3):334–342. doi:10.1111/jpi.12262.
   PubMed Web of Science ®Google Scholar
• Sun C, Liu L, Yu Y, Liu W, Lu L, Jin C, Lin X. Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. J Integr Plant Biol. 2015;57(6):550–561. doi:10.1111/jipb.12298.
   PubMed Web of Science ®Google Scholar
• Maxwell M, Johnson GN. Chlorophyll fluorescence–a practical guide. J Exp Bot. 2000;51(345):659–668. doi:10.1093/jexbot/51.345.659.
   PubMed Web of Science ®Google Scholar
• Heidari P, Amerian MR, Barcaccia G. Hormone profiles and antioxidant activity of cultivated and wild tomato seedlings under low-temperature stress. Agronomy-Basel. 2021;11(6):1146. doi:10.3390/agronomy11061146.
   Web of Science ®Google Scholar
• Van Der Ploeg A, Heuvelink E. Influence of sub-optimal temperature on tomato growth and yield: a review. J Hortic Sci Biotech. 2005;80(6):652–659. doi:10.1080/14620316.2005.11511994.
   Web of Science ®Google Scholar
• Soengas P, Rodriguez VM, Velasco P, Cartea ME. Effect of temperature stress on antioxidant defenses in Brassica oleracea. ACS Omega. 2018;3(5):5237–5243. doi:10.1021/acsomega.8b00242.
   PubMed Web of Science ®Google Scholar
• Ali B, Hayat S, Fariduddin Q, Ahmad A. 24-epibrassinolide protects against the stress generated by salinity and nickel in Brassica juncea. Chemosph. 2008;72(9):1387–1392. doi:10.1016/j.chemosphere.2008.04.012.
   PubMed Web of Science ®Google Scholar
• Mushtaq Z, Faizan S, Gulzar B, Mushtaq H, Bushra S, Hussain A, Hakeem KR. Changes in growth, photosynthetic pigments, cell viability, lipid peroxidation and antioxidant defense system in two varieties of chickpea (cicer arietinum L.) subjected to salinity stress. Phyton-Int J Exp Bot. 2022;91(1):149–168. doi:10.32604/phyton.2022.016231.
   Web of Science ®Google Scholar
• Kabay T. Effects of low tempertaures on enzyme activity, chlorophyll and ion contents in common bean genotypes. Appl Ecol Env Res. 2018;16(5):7271–7287. doi:10.15666/aeer/1605_72717287.
   Web of Science ®Google Scholar
• Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Lukasik I, Goltsev V, Ladle RJ. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant. 2016;38(4):102. doi:10.1007/s11738-016-2113-y.
   Web of Science ®Google Scholar
• Altaf MA, Shahid R, Ren MX, NaZ S, Altaf MM, Khan LU, Tiwari RK, Lal MK, Shahid MA, Kumar R, et al. Melatonin improves drought stress tolerance of tomato by modulating plant growth, root architecture, photosynthesis, and antioxidant defense system. Antioxidants. 2022;11(2):309. doi:10.3390/antiox11020309.
   Web of Science ®Google Scholar
• Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments. Plant Signal Behav. 2012;7(11):1456–1466. doi:10.4161/psb.21949.
   PubMedGoogle Scholar
• Huang Y, Wang S, Wang C, Ding G, Cai H, Shi L, Xu F. Induction of jasmonic acid biosynthetic genes inhibits arabidopsis growth in response to low boron. J Integr Plant Biol. 2021;63(5):937–948. doi:10.1111/jipb.13048.
   PubMed Web of Science ®Google Scholar
• Wang K, Bai ZY, Liang QY, Liu QL, Zhang L, Pan YZ, Liu GL, Jiang BB, Zhang F, Jia Y. Transcriptome analysis of chrysanthemum (dendranthema grandiflorum) in response to low temperature stress. BMC Genomics. 2018;19(1):319. doi:10.1186/s12864-018-4706-x.
   PubMedGoogle Scholar
• Duran Garzon C, Lequart M, Rautengarten C, Bassard S, Sellier-Richard H, Baldet P, Heazlewood JL, Gibon Y, Domon JM, Giauffret C, et al. Regulation of carbon metabolism in two maize sister lines contrasted for chilling tolerance. J Exp Bot. 2020;71(1):356–369. doi:10.1093/jxb/erz421.
   PubMed Web of Science ®Google Scholar
• Chen HY, Chen XL, Chai XF, Qiu YX, Gong C, Zhang ZZ, Wang TT, Zhang Y, Li JF, Wang AX. Effects of low temperature on mRNA and small RNA transcriptomes in solanum lycopersicoides leaf revealed by RNA-Seq. Biochem Bioph Res Co. 2015;464(3):768–773. doi:10.1016/j.bbrc.2015.07.029.
   PubMed Web of Science ®Google Scholar
• Ritonga FN, Ngatia JN, Wang Y, Khoso MA, Farooq U, Chen S. AP2/ERF, an important cold stress-related transcription factor family in plants: a review. Physiol Mol Biol Plants. 2021;27(9):1953–1968. doi:10.1007/s12298-021-01061-8.
   PubMed Web of Science ®Google Scholar
• Bhardwaj AR, Joshi G, Kukreja B, Malik V, Arora P, Pandey R, Shukla RN, Bankar KG, Katiyar-Agarwal S, Goel S, et al. Global insights into high temperature and drought stress regulated genes by RNA-Seq in economically important oilseed crop Brassica juncea. BMC Plant Biol. 2015;15(1):9. doi:10.1186/s12870-014-0405-1.
   PubMedGoogle Scholar
• Palmeros-Suárez PA, Massange-Sánchez JA, Martínez-Gallardo NA, Montero-Vargas JM, Gómez-Leyva JF, Délano-Frier JP. The overexpression of an amaranthus hypochondriacus NF-YC gene modifies growth and confers water deficit stress resistance in arabidopsis. Plant Sci. 2015;240:25–40. doi:10.1016/j.plantsci.2015.08.010.
   PubMed Web of Science ®Google Scholar
• Wu L, Chen X, Ren H, Zhang Z, Zhang H, Wang J, Wang X-C, Huang R. ERF protein JERF1 that transcriptionally modulates the expression of abscisic acid biosynthesis-related gene enhances the tolerance under salinity and cold in tobacco. Planta. 2007;226(4):815–825. doi:10.1007/s00425-007-0528-9.
   PubMed Web of Science ®Google Scholar
• Wu L, Zhang Z, Zhang H, Wang XC, Huang RJPP. Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Phusiol. 2008;148(4):1953–1963. doi:10.1104/pp.108.126813.
   PubMed Web of Science ®Google Scholar
• Zhang HW, Liu W, Wan LY, Li F, Dai LY, Li DJ, Zhang ZJ, Huang RF. Functional analyses of ethylene response factor JERF3 with the aim of improving tolerance to drought and osmotic stress in transgenic rice. Transgentic Res. 2010;19(5):809–818. doi:10.1007/s11248-009-9357-x.
   PubMed Web of Science ®Google Scholar
• Shi XY, Li T, Wang HY, Zhang RQ, Cao SJ, Zhang LL, Yao JG, Liu JF. Research progress of tomato MYB transcription factor. China Cucurbit Vegetables. 2023;36:9–14.
   Google Scholar
• Liang YF, Ma F, Li BY, Guo C, Hu TX, Zhang MK, Liang Y, Zhu JH, Zhan XQ. A bHLH transcription factor, SlbHLH96, promotes drought tolerance in tomato. Hortic Res. 2022;9:uhac198. doi:10.1093/hr/uhac198.
   PubMed Web of Science ®Google Scholar
• Abeynayake SW, Etzerodt TP, Jonaviciene K, Byrne S, Asp T, and Boelt B. Fructan metabolism and changes in fructan composition during cold acclimation in perennial ryegrass. Front Plant Sci. 2015;6:329. doi:10.3389/fpls.2015.00329.
   PubMed Web of Science ®Google Scholar
• Peng T, Zhu XF, Fan QJ, Sun PP, Liu JH. Identification and characterization of low temperature stress responsive genes in poncirus trifoliata by suppression subtractive hybridization. Gene. 2012;492(1):220–228. doi:10.1016/j.gene.2011.10.025.
   PubMed Web of Science ®Google Scholar
• Zhang YY, Zeng DW, Liu YH, Zhu WM. SlSPS, a sucrose phosphate synthase gene, mediates plant growth and thermotolerance in tomato. Horticulturae. 2022a;8(6):491. doi:10.3390/horticulturae8060491.
   Web of Science ®Google Scholar
• Mollavali M, Börnke F. Characterization of trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase genes of tomato (solanum lycopersicum L.) and analysis of their differential expression in response to temperature. Int J Mol Sci. 2022;23(19):11436. doi:10.3390/ijms231911436.
   PubMed Web of Science ®Google Scholar
• Mostofa MG, Hossain MA, Fujita M, Tran LS. Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep. 2015;5(1):11433. doi:10.1038/srep11433.
   PubMedGoogle Scholar
• Zuo SY, Li J, Gu WR, Wei S. Exogenous proline alleviated low temperature stress in maize embryos by optimizing seed germination, inner proline metabolism, respiratory metabolism and a hormone regulation mechanism. Agriculture-Basel. 2022;12(4):32. doi:10.3390/agriculture12040548.
   Web of Science ®Google Scholar
• Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K. Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett. 1999;461(3):205–10. doi:10.1016/S0014-5793(99)01451-9.
   PubMed Web of Science ®Google Scholar
• Ibragimova SM, Genaev MA, Kochetov AV, Afonnikov DA. Variability of leaf pubescence characteristics in transgenic tobacco lines with partial proline dehydrogenase gene suppression. Biol Plantarum. 2022;66:24–28. doi:10.32615/bp.2021.067.
   Web of Science ®Google Scholar