Abstract
Main conclusion
This report proves a cross talk between H2S and IAA in cold stress response, which has presented strong evidence that IAA acts as a downstream signal mediating the H2S-induced stress tolerance in cucumber seedlings.
Abstract
We evaluated changes in endogenous hydrogen sulfide (H2S) and indole-3-acetic acid (IAA) emission systems, and the interactive effect of exogenous H2S and IAA on chilling tolerance in cucumber seedlings. The results showed that chilling stress increased the activity and relative mRNA expression of l-/d-cysteine desulfhydrase (l-/d-CD), which in turn induced the accumulation of endogenous H2S. Similarly, the endogenous IAA system was triggered by chilling stress. We found that 1.0 mM sodium hydrosulfide (NaHS, an H2S donor) significantly enhanced the activity of flavin monooxygenase (FMO) and relative expression of FMO-like proteins (YUCCA2), which in turn elevated endogenous IAA levels in cucumber seedlings. However, IAA had little effects on activities of l-/d-CD and endogenous H2S levels. H2S-induced IAA production accompanied by increase in chilling tolerance, as shown by the decrease in stress-induced electrolyte leakage (EL) and reactive oxygen species (ROS) accumulation, and increase in gene expressions and enzyme activities of photosynthesis. 1-naphthylphthalamic acid (NPA, an IAA polar transport inhibitor) declined H2S-induced chilling tolerance and defense genes’ expression. However, scavenging of H2S had a little effect on IAA-induced chilling tolerance. These results suggest that IAA acting as a downstream signaling molecule is involved in the H2S-induced chilling tolerance in cucumber seedlings.
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Abbreviations
- AsA:
-
Ascorbic acid
- Asat:
-
Light-saturated photosynthetic rate
- CBF:
-
C-repeat-binding factor
- COR:
-
Cold responsive
- DHA:
-
Dehydroascorbic acid
- EL:
-
Electrolyte leakage
- FMO:
-
Flavin monooxygenase
- GSH:
-
Reduced glutathione
- GSSG:
-
Oxidized glutathione
- HT:
-
Hydroxylamine
- ICE:
-
Inducer of CBF expression
- Jmax:
-
Maximum regeneration rate of Ribulose-1, 5-bisphosphate carboxylase/oxygenase
- L-/D-CD:
-
l-/d-cysteine desulfhydrase
- NPA:
-
1-Naphthylphthalamic acid
References
Ali B, Gill RA, Yang S, Gill MB, Ali S, Rafiq MT, Zhou W (2014) Hydrogen sulfide alleviates cadmium-induced morpho-physiological and ultrastructural changes in Brassica napus. Ecotox Environ Safe 110:197–207
Bashri G, Prasad SM (2016) Exogenous IAA differentially affects growth, oxidative stress and antioxidants system in Cd stressed Trigonella foenum-graecum L. seedlings: toxicity alleviation by up-regulation of ascorbate-glutathione cycle. Ecotox Environ Safe 132:329–338
Ben-Amor M, Flores B, Latche A, Bouzayen M, Pech JC, Fomojaro F (1999) Inhibition of ethylene biosynthesis by antisense ACC oxidase RNA prevents chilling injury in Charentais cantaloupe melons. Plant Cell Environ 22:1579–1586
Beyer WF Jr, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566
Bi H, Dong X, Wu G, Wang M, Ai X (2015) Decreased TK activity alters growth, yield and tolerance to low temperature and low light intensity in transgenic cucumber plants. Plant Cell Rep 34:345–354
Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011a) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493
Chen S, Liu Z, Cui J, Ding J, Xia X, Liu D, Yu J (2011b) Alleviation of chilling-induced oxidative damage by salicylic acid pretreatment and related gene expression in eggplant seedlings. Plant Growth Regul 65:101–108
Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286
Cho UH, Park JO (2000) Mercury-induced oxidative stress in tomato seedlings. Plant Sci 156:1–9
Chongchatuporn U, Ketsa S, van Doorn WG (2013) Chilling injury in mango (Mangifera indica) fruit peel: relationship with ascorbic acid concentrations and antioxidant enzyme activities. Postharvest Biol Technol 86:409–417
Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64:1953–1966
Dong X, Bi H, Wu G, Ai X (2013) Drought-induced chilling tolerance in cucumber involves membrane stabilisation improved by antioxidant system. Int J Plant Prod 7:67–80
Du X, Jin Z, Liu D, Yang G, Pei Y (2017) Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana. Plant Physiol Biochem 120:112–119
Fang T, Cao Z, Li J, Shen W, Huang L (2014) Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol Biochem 76:44–51
Fang P, Yan M, Chi C, Wang M, Zhou Y, Zhou J, Shi K, Xia X, Foyer CH, Yu J (2019) Brassinosteroids act as a positive regulator of photoprotection in response to chilling stress. Plant Physiol 180:2061–2076
Fotopoulos V, Ziogas V, Tanou G, Molassiotis A (2010) Involvement of AsA/DHA and GSH/GSSG ratios in gene and protein expression and in the activation of defence mechanisms under abiotic stress conditions. In: Anjum NA, Chan M-T, Kumar S (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 265–302
Foyer C, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25
Galluzzi L, Kroemer G (2014) Conceptual background and bioenergetic/mitochondrial aspects of oncometabolism. Methods Enzymol 542
García-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984
Gong B, Miao L, Kong W, Bai JG, Wang X, Wei M, Shi Q (2014) Nitric oxide, as a downstream signal, plays vital role in auxin induced cucumber tolerance to sodic alkaline stress. Plant Physiol Biochem 83:258–266
Hancock JT (2019) Hydrogen sulfide and environmental stresses. Environ Exp Bot 161:50–56
Harrington HM, Smith IK (1980) Cysteine metabolism in cultured tobacco cells. Plant Physiol 65:151–155
Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of CBF expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924
Iglesias MJ, Terrile MC, Bartoli CG, D’Ippólito S, Casalongué CA (2010) Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol Biol 74:215–222
Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162
Jin Z, Pei Y (2015) Physiological implications of hydrogen sulfide in plants: pleasant exploration behind its unpleasant odour. Oxid Med Cell Longev. https://doi.org/10.1155/2015/397502
Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486
Jung H, Lee DK, Do Choi Y, Kim JK (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci 236:304–312
Ke Q, Wang Z, Ji CY, Jeong JC, Lee HS, Li H, Xu B, Deng X, Kwak SS (2015) Transgenic poplar expressing Arabidopsis YUCCA6 exhibits auxin-overproduction phenotypes and increased tolerance to abiotic stress. Plant Physiol Biochem 94:19–27
Kocsy G, Galiba G, Brunold C (2001) Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol Plant 113:158–164
Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts. The effect of hydrogen peroxide and of Paraquat. Biochem J 210:899–903
Levitt J (1962) A sulfhydryl-disulfide hypothesis of frost injury and resistance in plants. J Theor Biol 3:355–391
Li Q, Yu B, Gao Y, Dai AH, Bai JG (2011) Cinnamic acid pretreatment mitigates chilling stress of cucumber leaves through altering antioxidant enzyme activity. J Plant Physiol 168:927–934
Li Y, Xu J, Zheng L, Li M, Yan X, Luo Q (2014) Simultaneous determination of ten phytohormones in five parts of Sargasum fusiforme (Hary.) Seichell by high performance liquid chromatography-triple quadrupole mass spectrometry. Chin J Chromatogr 32:861–866
Li ZG, Xie LR, Li XJ (2015) Hydrogen sulfide acts as a downstream signal molecule in salicylic acid-induced heat tolerance in maize (Zea mays L.) seedlings. J Plant Physiol 177:121–127
Luo Z, Li D, Du R, Mou W (2015) Hydrogen sulfide alleviates chilling injury of banana fruit by enhanced antioxidant system and proline content. Sci Hortic 183:144–151
Mei Y, Chen H, Shen W, Shen W, Huang L (2017) Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol 17:162
Nagasawa T, Ishii T, Kumagai H, Yamada H (1985) d-cysteine desulfhydrase of Escherichia coli purification and characterization. Eur J Biochem 153:1–7
Nakano Y, Asada K (1987) Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol 28:131–140
Omran RG (1980) Peroxide levels and the activities of catalase, peroxidase, and indoleaceticacid oxidase during and after chilling cucumber seedlings. Plant Physiol 65:407–408
Park HC, Cha JY, Yun DJ (2013) Roles of YUCCAs in auxin biosynthesis and drought stress responses in plants. Plant Signal Behav 8:e24495
Qiao Z, Jing T, Jin Z, Liang Y, Zhang L, Liu Z, Liu D, Pei Y (2016) CDPKs enhance Cd tolerance through intensifying H2S signal in Arabidopsis thaliana. Plant Soil 398:99–110
Rahman A (2013) Auxin: a regulator of cold stress response. Physiol Plant 147:28–35
Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB, Baskin TI (2007) Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J 50:514–528
Rao IM, Terry N (1989) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet: I. Changes in growth, gas exchange, and Calvin cycle enzymes. Plant Physiol 90:814–819
Riemenschneider A, Nikiforova V, Hoefgen R, De Kok LJ, Papenbrock J (2005) Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiol Biochem 43:473–483
Scuffi D, Alvarez C, Laspina N, Gotor C, Lamattina L, García-Mata C (2014) Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166:2065–2076
Sekiya J, Schmidt A, Wilson LG, Filner P (1982) Emission of hydrogen sulfide by leaf tissue in response to L-cysteine. Plant Physiol 70:430–436
Semeniuk P, Moline HE, Abbott JAA (1986) Comparison of the effects of ABA and an antitranspirant on chilling injury of coleus, cucumbers, and dieffenbachia. J Am Soc Hortic Sci 111:866–868
Sharma L, Dalal M, Verma RK, Kumar SVV, Yadav SK, Pushkar S, Kushwaha SR, Bhowmik A, Chinnusamy V (2018) Auxin protects spikelet fertility and grain yield under drought and heat stresses in rice. Environ Exp Bot 150:9–24
Shi H, Chen L, Ye T, Liu X, Ding K, Chan Z (2014) Modulation of auxin content in Arabidopsis confers improved drought stress resistance. Plant Physiol Biochem 82:209–217
Shi Y, Ding Y, Yang S (2015) Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiol 56:7–15
Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21:3823–3838
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455
Singh S, Prasad SM (2015) IAA alleviates Cd toxicity on growth, photosynthesis and oxidative damages in eggplant seedlings. J Plant Growth Regul 77:87–98
Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-facetted molecule. Curr Opin Plant Biol 3:229–235
Stuiver CEE, De Kok LJ, Kuiper PJC (1992) Freezing tolerance and biochemical changes in wheat shoots as affected by H2S fumigation. Plant Physiol Biochem 30:47–55
Szalai G, Kellős T, Galiba G, Kocsy G (2009) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80
Wang AG (1990) Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. Plant Physiol Commun 26:55–57
Wang C, Yang A, Yin H, Zhang J (2008) Influence of water stress on endogenous hormone contents and cell damage of maize seedlings. J Integr Plant Biol 50:427–434
Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119
Wu GX, Cai BB, Zhou CF, Li DD, Bi HG, Ai XZ (2016) Hydrogen sulfide-induced chilling tolerance of cucumber and involvement of nitric oxide. J Plant Biol Res 5:58–69
Wu GX, Li DD, Sun CC, Sun SN, Liu FJ, Bi HG, Ai XZ (2017) Hydrogen sulfide interacts with Ca2+ to enhance chilling tolerance of cucumber seedlings. Chin J Biochem Mol Biol 33:1037–1046
Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009) Hydrogen Sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094
Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567
Zhang XL, Jia XF, Yu B, Gao Y, Bai JG (2011) Exogenous hydrogen peroxide influences antioxidant enzyme activity and lipid peroxidation in cucumber leaves at low light. Sci Hortic 129:656–662
Zhang L, Pei Y, Wang H, Jin Z, Liu Z, Qiao Z, Fang H, Zhang Y (2015) Hydrogen sulfide alleviates cadmium-induced cell death through restraining ROS accumulation in roots of Brassica rapa L. ssp. pekinensis. Oxid Med Cell Longev, Art. ID 804603. doi: 10.1155/2015/804603
Zörb C, Geilfus CM, Mühling KH, Ludwig-Müller J (2013) The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J Plant Physiol 170:220–224
Acknowledgements
This work is supported by The National Key Research and Development Program of China (2018YFD1000800), The National Science Foundation of China (31572170), The Special Fund of Modern Agriculture Industrial Technology System of Shandong Province in China (SDAIT-05–10), and The Funds of Shandong ‘Double Tops’ Program (SYL2017YSTD06).
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Zhang, XW., Liu, FJ., Zhai, J. et al. Auxin acts as a downstream signaling molecule involved in hydrogen sulfide-induced chilling tolerance in cucumber. Planta 251, 69 (2020). https://doi.org/10.1007/s00425-020-03362-w
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DOI: https://doi.org/10.1007/s00425-020-03362-w