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Exogenous 5-aminolevulinic acid pretreatment ameliorates oxidative stress triggered by low-temperature stress of Solanum lycopersicum

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Abstract

Low temperature is an important limiting factor in tomato production in early spring and winter. 5-Aminolevulinic acid (ALA) protects crops against varied abiotic stresses. However, the methodology to precisely use ALA to increase the cold tolerance in tomatoes is still not fully known. We therefore explored the effects of ALA concentration, application period, and dose on membrane lipid peroxidation, antioxidation, photosynthesis, and plant growth in different tomato cultivars (Zhongza No. 9, ZZ and Jinpeng No. 1, JP) at low-temperature stress. Results revealed that low temperature caused plants oxidative damage and growth inhibition in both ZZ and JP plants. The ROS (hydrogen peroxide and superoxide anion) accumulation and membrane lipid peroxidation (malondialdehyde content and the relative electrical conductivity) were more remarkable in JP plants than ZZ plants under low temperature. The catalase (CAT) and ascorbate–glutathione cycle (AsA–GSH) induced by ALA reliably eliminated excessive ROS to maintain the redox balance in both tomato cultivars under low-temperature stress. In AsA–GSH cycle, AsA regeneration was mainly catalyzed by dehydroascorbate reductase (DHAR) and monodehydroascorbate reductase (MDHAR), from dehydroascorbate (DHA) to AsA and monodehydroascorbate (MDA) to AsA in ZZ plants, while AsA regeneration in JP plants was mostly catalyzed by DHAR, from DHA to AsA. The ALA optimum concentration was 25 mg L−1. The tomato plants with five true leaves pretreated with 6 mL ALA were more effective than spraying after cold occurred. In conclusion, the two tomato varieties illustrated different capacities to bear low-temperature stress. And ZZ plants were more tolerant to low temperature than JP plants. Precise ALA pretreatment observably alleviated low temperature induced-damage via CAT and AsA–GSH cycle in both cultivars. The regeneration of AsA in AsA–GSH cycle may be more comprehensive in ZZ plants than JP plants, to better tolerate low-temperature stress.

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References

  • Akram NA, Ashraf M (2013) Regulation in plant stress tolerance by a potential plant growth regulator, 5-aminolevulinic acid. J Plant Growth Regul 32:663–679

    Article  CAS  Google Scholar 

  • Ali B, Xu X, Gill RA, Yang S, Ali S, Tahir M, Zhou WJ (2014) Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crop Prod 52:617–626

    Article  CAS  Google Scholar 

  • An YY, Li J, Duan CH, Liu LB, Sun YP, Cao RX, Wang LJ (2016a) 5-Aminolevulinic acid thins pear fruits by inhibiting pollen tube growth via Ca2+-ATPase-mediated Ca2+ efflux. Front Plant Sci 7:121

    PubMed  PubMed Central  Google Scholar 

  • An YY, Liu LB, Chen LH, Wang LJ (2016b) ALA inhibits ABA-induced stomatal closure via reducing H2O2 and Ca2+ levels in guard cells. Front Plant Sci 7:482

    PubMed  PubMed Central  Google Scholar 

  • Apitz J, Nishimura K, Schmied J, Wolf A, Hedtke B, van Wijk KJ, Grimm B (2016) Posttranslational control of ALA synthesis includes GluTR degradation by Clp protease and stabilization by GluTR-binding protein. Plant Physiol 170(4):2040–2051

    Article  CAS  Google Scholar 

  • Balestrasse KB, Tomaro ML, Batlle A, Noriega GO (2010) The role of 5-aminolevulinic acid in the response to cold stress in soybean plants. Phytochemistry 71:2038–2045

    Article  CAS  Google Scholar 

  • Barrero-Gil J, Huertas R, Rambla JL, Granell A, Salinas J (2016) Tomato plants increase their tolerance to low temperature in a chilling acclimation process entailing comprehensive transcriptional and metabolic adjustments. Plant Cell Environ 39(10):2303–2318

    Article  CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Article  CAS  Google Scholar 

  • Cheng F, Lu JY, Gao M, Shi K, Kong QS, Huang Y, Bie ZL (2016) Redox signaling and CBF-responsive pathway are involved in salicylic acid-improved photosynthesis and growth under chilling stress in watermelon. Front Plant Sci 7:01519

    Google Scholar 

  • Czarnecki O, Hedtke B, Melzer M, Rothbart M, Richter A, Schroter Y, Pfannschmidt T, Grimm B (2011) An arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. Plant Cell 23:4476–4491

    Article  CAS  Google Scholar 

  • Dietz KJ, Mittler R, Noctor G (2016) Recent progress in understanding the role of reactive oxygen species in plant cell signaling. Plant Physiol 171:1535–1539

    Article  CAS  Google Scholar 

  • Dutilleul C, Garmier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, Paepe Rd (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1212–1226

    Article  CAS  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  Google Scholar 

  • Guo XT, Li YS, Yu XC (2012) Promotive effects of 5-aminolevulinic acid on photosynthesis and chlorophyll fluorescence of tomato seedlings under suboptimal low temperature and suboptimal photon flux density stress. Hortic Sci 39(2):97–99

    Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223

    Article  CAS  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hodgins RR, Öquist G (1989) Porphyrin metabolism in chill-stressed seedlings of Scots pine (Pinus sylvestris). Physiol Plant 77:620–624

    Article  CAS  Google Scholar 

  • Hotta Y, Tanaka T, Takaoka H, Takeuchi Y, Konnai M (1997) New physiological effects of 5-aminolevulinic acid in plants: the increase of photosynthesis, chlorophyll content, and plant growth. Biosci Biotechnol Biochem 61:2025–2028

    Article  CAS  Google Scholar 

  • Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195:737–751

    Article  CAS  Google Scholar 

  • Korkmaz A, Korkmaz Y, Demirkıran AR (2010) Enhancing chilling stress tolerance of pepper seedlings by exogenous application of 5-aminolevulinic acid. Environ Exp Bot 67:495–501

    Article  CAS  Google Scholar 

  • Li D, Zhang J, Sun W, Li Q, Dai A, Bai J (2011) 5-Aminolevulinic acid pretreatment mitigates drought stress of cucumber leaves through altering antioxidant enzyme activity. Sci Hortic 130:820–828

    Article  CAS  Google Scholar 

  • Li QY, Lei S, Du KB, Li LZ, Pang XF, Wang ZC, Wei M, Fu S, Hu LM, Xu L (2016) RNA-seq based transcriptomic analysis uncovers α-linolenic acid and jasmonic acid biosynthesis pathways respond to cold acclimation in Camellia japonica. Sci Rep 6:36463

    Article  CAS  Google Scholar 

  • Li H, Chang JJ, Zheng JX, Dong YC, Liu Q, Yang XZ, Wei CH, Zhang Y, Ma JX, Zhang X (2017) Local melatonin application induces cold tolerance in distant organs of Citrullus lanatus L. via long distance transport. Sci Rep 7:40858

    Article  CAS  Google Scholar 

  • Liu D, Kong DD, Fu XK, Ali B, Xu L, Zhou WJ (2016) Influence of exogenous 5-aminolevulinic acid on chlorophyll synthesis and related gene expression in oilseed rape de-etiolated cotyledons under water-deficit stress. Photosynthetica 54:468–474

    Article  CAS  Google Scholar 

  • Liu T, Hu XH, Zhang J, Zhang JH, Du QJ, Li JM (2018a) H2O2 mediates ALA-induced glutathione and ascorbate accumulation in the perception and resistance to oxidative stress in Solanum lycopersicum at low temperatures. BMC Plant Biol 18:34

    Article  Google Scholar 

  • Liu T, Xu JJ, Li JM, Hu XH (2018b) NO is involved in JA- and H2O2-mediated ALA-induced oxidative stress tolerance at low temperatures in tomato. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot

    Article  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    Article  CAS  Google Scholar 

  • Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337

    Article  CAS  Google Scholar 

  • Naeem MS, Jin ZL, Wan GL, Liu D, Liu HB, Yoneyama K, Zhou WJ (2010) 5-Aminolevulinic acid improves photosynthetic gas exchange capacity and ion uptake under salinity stress in oilseed rape (Brassica napus L.). Plant Soil 332:405–415

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous spermidine alleviates low temperature injury in mung bean (Vigna radiata L.) seedlings by modulating ascorbate–glutathione and glyoxalase pathway. Int J Mol Sci 16(12):30117–30132

    Article  CAS  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ 39:1140–1160

    Article  CAS  Google Scholar 

  • op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

    Article  Google Scholar 

  • Qu T, Liu RF, Wang W, An L, Chen T, Liu GX, Zhao ZG (2011) Brassinosteroids regulate pectin methylesterase activity and AtPME41 expression in Arabidopsis under chilling stress. Cryobiology 63(2):111–117

    Article  CAS  Google Scholar 

  • Richter AS, Grimm B (2013) Thiol-based redox control of enzymes involved in the tetrapyrrole biosynthesis pathway in plants. Front Plant Sci 4:371

    Article  Google Scholar 

  • Strain HH, Svec WA (1966) Extraction, separation, estimation and isolation of the chlorophylls. In: Vernon LP, Seeley GR (eds) The chlorophylls. Academic Press, New York, pp 21–66

    Chapter  Google Scholar 

  • Sun YP, Zhang ZP, Wang LJ (2009) Promotion of 5-aminolevulinic acid treatment on leaf photosynthesis is related with increase of antioxidant enzyme activity in watermelon seedlings grown under shade condition. Photosynthetica 47:347–354

    Article  CAS  Google Scholar 

  • Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Boil 9(3):248–255

    Article  CAS  Google Scholar 

  • Tewari AK, Tripathy BC (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858

    Article  CAS  Google Scholar 

  • von Wettstein D, Gough S, Kananagara CG (1995) Chlorophyll biosynthesis. Plant Cell 7:1039–1105

    Article  Google Scholar 

  • Wang P, Grimm B (2015) Organization of chlorophyll biosynthesis and insertion of chlorophyll into the chlorophyll-binding proteins in chloroplasts. Photosynth Res 126(2–3):189–202

    Article  CAS  Google Scholar 

  • Wang LJ, Jiang WB, Huang BJ (2004) Promotion of 5-aminolevulinic acid on photosynthesis of melon (Cucumis melo) seedlings under low light and chilling stress conditions. Physiol Plant 121:258–264

    Article  CAS  Google Scholar 

  • Wang LJ, Jiang WB, Liu H, Liu WQ, Kang L, Hou XL (2005) Promotion by 5-aminolevulinic acid of germination of pakchoi (Brassica campestris ssp. chinensis var. communis Tsen et Lee) seeds under salt stress. J Integr Plant Biol 47:1084–1091

    Article  CAS  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Montagu MV, Inzé D, Camp WV (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16(16):4806–4816

    Article  CAS  Google Scholar 

  • Willems P, Mhamdi A, Stael S, Storme V, Kerchev P, Noctor G, Gevaert K, Van Breusegem F (2016) The ROS wheel: refining ROS transcriptional footprints. Plant Physiol 171:1720–1733

    Article  Google Scholar 

  • Yang ZM, Chang ZL, Sun LH, Yu JJ, Huang BR (2014) Physiological and metabolic effects of 5-aminolevulinic acid for mitigating salinity stress in creeping bentgrass. PLoS One 9:e116283

    Article  Google Scholar 

  • Zhou WJ, Leul M (1998) Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regul 26:41–47

    Article  CAS  Google Scholar 

  • Zhou Y, Zeng LT, Fu XM, Mei X, Cheng SH, Liao YY, Deng RF, Xu X, Jiang YM, Duan XW, Baldermann S, Yang ZY (2016) The sphingolipid biosynthetic enzyme Sphingolipid delta8 desaturase is important for chilling resistance of tomato. Sci Rep 6:38742

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National High-tech R&D Program of China (863 Program) (2013AA103004), the China Agriculture Research System (CARS-23-C-05) and the National Natural Science Foundation of China (31772359).

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Correspondence to Jianming Li or Xiaohui Hu.

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Communicated by J. Gao.

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Liu, T., Xu, J., Zhang, J. et al. Exogenous 5-aminolevulinic acid pretreatment ameliorates oxidative stress triggered by low-temperature stress of Solanum lycopersicum. Acta Physiol Plant 40, 210 (2018). https://doi.org/10.1007/s11738-018-2788-3

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