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Exogenous application of 5-aminolevulinic acid on wheat seedlings under drought stress enhances the transcription of psbA and psbD genes and improves photosynthesis

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Abstract

The compound 5-aminolevulinic acid (ALA) is an essential precursor for the biosynthesis of porphyrins, including chlorophyll, heme, and cytochromes. The protective effects of ALA on photosynthesis and the expression of photosynthetic genes in wheat under drought stress are not well understood. Two wheat cultivars, drought-tolerant Aikang-58 and drought-sensitive Chinese Spring, were exposed to drought stress induced by 20% polyethylene glycol (PEG-6000) after foliar pretreatment with ALA for 3 days. The results showed that exogenous application of ALA protected the drought-stressed wheat seedlings by significantly inhibiting the decrease in relative water and chlorophyll contents. The ALA-mediated alleviation of stress was similar between the drought-tolerant and drought-sensitive wheat cultivars. Meanwhile, compared to seedlings under drought treatment alone, the ALA-pre-treated wheat seedlings under drought stress maintained higher photosystem II (PSII) functional indexes. The ALA pretreatment reduced the drought-driven accumulation of both H2O2 and ABA and increased the stomatal conductance. Real-time PCR analysis showed that the psbA and psbD gene transcripts were both upregulated under drought stress following ALA pretreatment. The present study suggests that the exogenous foliar application of ALA alleviates the drought stress on wheat seedlings, which is associated with the enhancement of PSII function by inducing chlorophyll synthesis and psbA and psbD transcription. Moreover, the protective effect of ALA pretreatment was not related to the decline in stomatal conductance caused by ABA or H2O2 accumulation.

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Abbreviations

ALA:

5-Aminolevulinic acid

ABA:

Abscisic acid

ANOVA:

One-way analysis of variance

CK:

Control

C T :

Cycle threshold

ELISA:

Enzyme-linked immunosorbent assay

Fv/Fm:

Maximum efficiency of PSII photochemistry

g s :

Stomatal conductance

H2O2 :

Hydrogen peroxide

PEG:

Polyethylene glycol

PPFD:

Photosynthetic photon flux density

P n :

Net photosynthetic rate

PSII:

Photosystem II

ΦPSII:

Actual quantum yield

qN:

Non-photochemical quenching coefficient

qP:

Photochemical quenching coefficient

RWC:

Relative water contents

References

  • Ahmad R, Ali S, Hannan F, Rizwan M, Iqbal M, Hassan Z, Akram NA, Maqbool S, Abbas F (2017) Promotive role of 5-aminolevulinic acid on chromium-induced morphological, photosynthetic, and oxidative changes in cauliflower (Brassica oleracea botrytis L.). Environ Sci Pollut Res 24:8814–8824

    Article  CAS  Google Scholar 

  • 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 

  • Akram NA, Iqbal M, Muhammad A, Ashraf M, Al-Qurainy F, Shafiq S (2018) Aminolevulinic acid and nitric oxide regulate oxidative defense and secondary metabolisms in canola (Brassica napus L.) under drought stress. Protoplasma 255:163–174

    Article  PubMed  CAS  Google Scholar 

  • Ali B, Wang B, Ali S, Ghani M, Hayat M, Yang C, Xu L, Zhou W (2013) 5-Aminolevulinic acid ameliorates the growth, photosynthetic gas exchange capacity, and ultrastructural changes under cadmium stress in Brassica napus L. J Plant Growth Regul 32:604–614

    Article  CAS  Google Scholar 

  • Al-Thabet S (2006) Promotive effect of 5-aminolevulinic acid on growth and yield of wheat grown under dry conditions. J Agron 5:45–49

    Article  Google Scholar 

  • Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bano A, Ullah F, Nosheen A (2012) Role of abscisic acid and drought stress on the activities of antioxidant enzymes in wheat. Plant Soil Environ 58:181–185

    Article  CAS  Google Scholar 

  • Bi A, Fan J, Hu Z, Wang G, Amombo E, Fu J, Hu T (2016) Differential acclimation of enzymatic antioxidant metabolism and photosystem II photochemistry in tall fescue under drought and heat and the combined stresses. Front Plant Sci 7:453

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen YE, Liu WJ, Su YQ, Cui JM, Zhang ZW, Yuan M, Zhang HY, Yuan S (2016) Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana. Physiol Plant 158:225–235

    Article  PubMed  CAS  Google Scholar 

  • Chen G, Fan PS, Feng WM, Guan AQ, Lu YY, Wan YL (2017) Effects of 5-aminolevulinic acid on nitrogen metabolism and ion distribution of watermelon seedlings under salt stress. Russ J Plant Physiol 64:116–123

    Article  CAS  Google Scholar 

  • Cheng F, Liu YF, Lu GY, Zhang XK, Xie LL, Yuan CF, Xu BB (2016) Graphene oxide modulates root growth of Brassica napus L. and regulates ABA and IAA concentration. J Plant Physiol 193:57–63

    Article  PubMed  CAS  Google Scholar 

  • Danquah A, de Zelicourt A, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32:40–52

    Article  PubMed  CAS  Google Scholar 

  • Eshaghi S, Andersson B, Barber J (1999) Isolation of a highly active PSII-LHCII supercomplex from thylakoid membranes by a direct method. FEBS Lett 446:23–26

    Article  PubMed  CAS  Google Scholar 

  • Guan XK, Song L, Wang TC, Turner NC, Li FM (2015) Effect of drought on the gas exchange, chlorophyll fluorescence and yield of six different-era spring wheat cultivars. J Agron Crop Sci 201:253–266

    Article  CAS  Google Scholar 

  • Han R, Gao G, Li Z, Dong Z, Guo Z (in press) Effects of exogenous 5-aminolevulinic acid on seed germination of alfalfa (Medicago varia Martyn.) under drought stress. Grassland Sci. https://doi.org/10.1111/grs.12189

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. In: Circular. California Agricultural Experiment Station 347, 2nd edn., pp 4–32

  • Kiss E, Kos PB, Chen M, Vass I (2012) A unique regulation of the expression of the psbA, psbD, and psbE genes, encoding the D1, D2 and cytochrome b559 subunits of the Photosystem II complex in the chlorophyll d containing cyanobacterium Acaryochloris marina. Biochim Biophys Acta 1817:1083–1094

    Article  PubMed  CAS  Google Scholar 

  • Kooten O, Snel JF (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  PubMed  Google Scholar 

  • Kosar F, Akram NA, Ashraf M (2015) Exogenously-applied 5-aminolevulinic acid modulates some key physiological characteristics and antioxidative defense system in spring wheat (Triticum aestivum L.) seedlings under water stress. S Afr J Bot 96:71–77

    Article  CAS  Google Scholar 

  • Liu WJ, Yuan S, Zhang NH, Lei T, Duan HG, Liang HG, Lin HH (2006) Effect of water stress on photosystem II in two wheat cultivars. Biol Plant 50:597–602

    Article  CAS  Google Scholar 

  • Liu D, Pei ZF, Naeem MS, Ming DF, Liu HB, Khan F, Zhou WJ (2011) 5-Aminolevulinic acid activates antioxidative defence system and seedling growth in Brassica napus L. under water-deficit stress. J Agron Crop Sci 197:284–295

    Article  CAS  Google Scholar 

  • Liu D, Wu L, Naeem MS, Liu H, Deng X, Xu L, Zhang F, Zhou W (2013) 5-Aminolevulinic acid enhances photosynthetic gas exchange, chlorophyll fluorescence and antioxidant system in oilseed rape under drought stress. Acta Physiol Plant 35:2747–2759

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mohammadi H, Moradi F (2016) Effects of growth regulators on enzymatic and non-enzymatic antioxidants in leaves of two contrasting wheat cultivars under water stress. Braz J Bot 39:495–505

    Article  Google Scholar 

  • Nishiyama Y, Murata N (2014) Revised scheme for the mechanism of photoinhibition and its application to enhance the abiotic stress tolerance of the photosynthetic machinery. Appl Microbiol Biotechnol 98:8777–8796

    Article  PubMed  CAS  Google Scholar 

  • Niu K, Ma X, Liang G, Ma H, Jia Z, Liu W, Yu Q (2017) 5-Aminolevulinic acid modulates antioxidant defense systems and mitigates drought-induced damage in Kentucky bluegrass seedlings. Protoplasma 254:2083–2094

    Article  PubMed  CAS  Google Scholar 

  • Phung TH, Jung S (2014) Perturbed porphyrin biosynthesis contributes to differential herbicidal symptoms in photodynamically stressed rice (Oryza sativa) treated with 5-aminolevulinic acid and oxyfluorfen. Pestic Biochem Physiol 116:103–110

    Article  PubMed  CAS  Google Scholar 

  • Porra R, Thompson W, Kriedemann P (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophy Acta Bioenergy 975:384–394

    Article  CAS  Google Scholar 

  • Rao DE, Chaitanya K (2016) Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants. Biologia Plant 60:201–218

    Article  CAS  Google Scholar 

  • Sarijeva G, Knapp M, Lichtenthaler HK (2007) Differences in photosynthetic activity, chlorophyll and carotenoid levels, and in chlorophyll fluorescence parameters in green sun and shade leaves of Ginkgo and Fagus. J Plant Physiol 164:950–955

    Article  PubMed  CAS  Google Scholar 

  • Sheteiwy M, Shen H, Xu J, Guan Y, Song W, Hu J (2017) Seed polyamines metabolism induced by seed priming with spermidine and 5-aminolevulinic acid for chilling tolerance improvement in rice (Oryza sativa L.) seedlings. Environ Exp Bot 137:58–72

    Article  CAS  Google Scholar 

  • Song JX, Anjum SA, Zong XF, Yan R, Wang L, Yang AJ, Ashraf U, Zohaib A, Lv J, Zhang Y, Dong YF, Wang SG (2017) Combined foliar application of nutrients and 5-aminolevulinic acid (ALA) improved drought tolerance in Leymus chinensis by modulating its morpho-physiological characteristics. Crop Past Sci 68:474–482

    Article  CAS  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  PubMed  CAS  Google Scholar 

  • Wang YX, Suo B, Zhao TF, Qu XF, Yuan LG, Zhao XJ, Zhao HJ (2011) Effect of nitric oxide treatment on antioxidant responses and psbA gene expression in two wheat cultivars during grain filling stage under drought stress and rewatering. Acta Physiol Plant 33:1923–1932

    Article  CAS  Google Scholar 

  • Wang YX, Liu SC, Zhang HL, Zhao YD, Zhao HJ, Liu HS (2014) Glycine betaine application in grain filling wheat plants alleviates heat and high light-induced photoinhibition by enhancing the psbA transcription and stomatal conductance. Acta Physiol Plant 36:2195–2202

    Article  CAS  Google Scholar 

  • Wang YX, Yang M, Wei SM, Qin FJ, Zhao HJ, Suo B (2017) Identification of circular RNAs and their targets in leaves of Triticum aestivum L. under dehydration stress. Front Plant Sci 7:2024

    PubMed  PubMed Central  Google Scholar 

  • Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525

    Article  PubMed  CAS  Google Scholar 

  • Xiong JL, Wang HC, Tan XY, Zhang CL, Naeem MS (2018) 5-aminolevulinic acid improves salt tolerance mediated by regulation of tetrapyrrole and proline metabolism in Brassica napus L. seedlings under NaCl stress. Plant Physiol Biochem 124:88–99

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto Y, Aminaka R, Yoshioka M, Khatoon M, Komayama K, Takenaka D, Yamashita A, Nijo N, Inagawa K, Morita N, Sasaki T (2008) Quality control of photosystem II: impact of light and heat stresses. Photosynth Res 98:589–608

    Article  PubMed  CAS  Google Scholar 

  • Yang M, Qin B, Ma X, Wang P, Li M, Chen L, Chen L, Sun A, Wang Z, Yin Y (2016) Foliar application of sodium hydrosulfide (NaHS), a hydrogen sulfide (H2S) donor, can protect seedlings against heat stress in wheat (Triticum aestivum L.). J Integr Agric 15:2745–2758

    Article  CAS  Google Scholar 

  • Yuan S, Liu WJ, Zhang NH, Wang MB, Liang HG, Lin HH (2005) Effects of water stress on major photosystem II gene expression and protein metabolism in barley leaves. Physiol Plant 125:464–473

    Article  CAS  Google Scholar 

  • Zhao H, Zhao X, Ma P, Wang Y, Hu W, Li L, Zhao Y (2011) Effects of salicylic acid on protein kinase activity and chloroplast D1 protein degradation in wheat leaves subjected to heat and high light stress. Acta Ecol Sin 31:259–263

    Article  Google Scholar 

  • Zhao YY, Yan F, Hu LP, Zhou XT, Zou ZR, Cui LR (2015) Effects of exogenous 5-aminolevulinic acid on photosynthesis, stomatal conductance, transpiration rate, and PIP gene expression of tomato seedlings subject to salinity stress. Genet Mol Res 14:6401–6412

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (Grant No. U1704103), the Education Department of Henan Province (Grant No. 16A210030), the Sci-tech Innovation Foundation of Henan Agricultural University (Grant No. KJCX2016A06), and the National Innovation and Entrepreneurship Training Program of Undergraduate Student in Henan University (201710466013).

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YW and HZ contributed to the experimental design and writing of this manuscript. YW, SW, XS, and JW contributed on the performance of experiments. BS and FQ contributed to the data analysis.

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Correspondence to Yuexia Wang or Huijie Zhao.

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Wang, Y., Wei, S., Wang, J. et al. Exogenous application of 5-aminolevulinic acid on wheat seedlings under drought stress enhances the transcription of psbA and psbD genes and improves photosynthesis. Braz. J. Bot 41, 275–285 (2018). https://doi.org/10.1007/s40415-018-0455-y

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