Skip to main content

Advertisement

SpringerLink
Log in

Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Hydrogen sulfide (H2S) is considered to be the third gaseous signaling molecule after NO and CO, and it plays an active role in regulating the physiological processes of plants and animals. In this work, rice cultivar ‘IIyou 084’ seedlings were treated with NaHS, which is a donor of H2S, for 10 days, and its effects on growth and physiology, including photosynthesis, photorespiration, chlorophyll fluorescence, and stomata, were investigated. The data revealed that 0.01 mM of H2S improved rice biomass and chlorophyll content, while higher concentrations of H2S had an adverse effect on these parameters. Photosynthetic rate, stomatal conductance, and ribulose-1,5-bisphosphate carboxylase (EC 4.1.1.39) activity also increased under 0.01 mM H2S treatment. However, photosynthetic oxygen evolution rate, photosynthetic electron transfer, and photochemical efficiency of PSII were not affected by H2S treatment. In addition, photosynthesis oxygen sensitivity, CO2 compensation point, and glycolate oxidase (EC 1.1.3.1) activity reduced by H2S treatment, and thus photorespiration was down-regulated. Under light, stomatal aperture and density increased by treatment with 0.01 mM H2S. On the basis of these results, it can be deduced that 0.01 mM of H2S treatment improved photosynthesis in rice by increasing its stomatal aperture and density, which may result from reduced photorespiration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

Amax:

Maximum photosynthetic rate

AQE:

Apparent quantum efficiency

Chl:

Chlorophyll

Ca:

Atmospheric CO2 concentration

Ci:

Intercellular CO2 concentration

CE:

Carboxylation efficiency

ETR:

Relative electron transport rate

Fo:

Initial fluorescence

Fm:

The maximum fluorescence

Fm′:

Maximal fluorescence at actinic light

Fv′:

Variable fluorescence at actinic light

Fv/Fm:

Dark-adapted maximum quantum yield of PSII

Fv′/Fm′:

Light-adapted maximum quantum yield of PSII

GO:

Glycolate oxidase

Gs:

Stomatal conductance

H2S:

Hydrogen sulfide

Ls:

Stomatal limitation value

NaHS:

Sodium hydrosulfide

PSII:

Photosystem II

Pn:

Net photosynthetic rate

PGK:

3-Phosphoglygeric phosphokinase

RuBP:

Ribulose-1,5-bisphosphate

RuBPCase:

Ribulose-1,5-bisphosphate carboxylase

Tr:

Transpiration rate

WUE:

Water-use efficiency

Г:

CO2 compensation point

ΦPSII:

Light-adapted actual photochemical yield of PSII

References

  • Bertolde FZ, Almeida AAF, Pirovani CP, Gomes FP, Ahnetr D, Baligar VC, Valle RR (2012) Physiological and biochemical responses of Theobroma cacao L. genotypes to flooding. Photosynthetica 50(3):447–457. doi:10.1007/s11099-012-0052-4

    Article  CAS  Google Scholar 

  • Booker FL, Reid CD, Brunschön-Harti S, Fiscus EL, Miller JE (1997) Photosynthesis and photorespiration in soybean [Glycine max (L.) Merr.] chronically exposed to elevated carbon dioxide and ozone. J Exp Bot 48(315):1843–1852. doi:10.1093/jxb/48.10.1843

    Article  CAS  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir LS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122. doi:10.1111/j.1365-313X.2005.02615.x

    Article  CAS  PubMed  Google Scholar 

  • Büssis D, Groll UV, Fisahn J, Altmann T (2006) Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions. Funct Plant Biol 33(11):1037–1043. doi:10.1071/FP06078

    Article  Google Scholar 

  • Campbell CR, Plank CO (1998) Preparation of plant tissue for laboratory analysis. In: Kalra YP (ed) Handbook of reference methods for plant analysis. CRC Press LLC, Boca Raton, pp 39–40

    Google Scholar 

  • Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 63(13):4481–4493. doi:10.1093/jxb/err145

    Article  Google Scholar 

  • Cheng W, Zhang L, Jiao CJ, Su M, Yang T, Zhou LN, Peng RY, Wang RR, Wang CY (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286. doi:10.1016/j.plaphy.2013.05.042

    Article  CAS  PubMed  Google Scholar 

  • 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(7):1953–1966. doi:10.1093/jxb/ert055

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Coyne PI, Bingham GE (2012) Photosynthesis and stomatal light responses in snap beans exposed to hydrogen sulfide and ozone. J Air Pollut Control Assoc 28(11):1119–1123. doi:10.1080/00022470.1978.10470715

    Article  Google Scholar 

  • Dawood M, Cao FB, Jahangir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminium uptake and oxidative stress in barley. J Hazard Mater 209(210):121–128. doi:10.1016/j.jhazmat.2011.12.076

    Article  PubMed  Google Scholar 

  • García-Mata C, Lamattina L (2010) Hydrogen sulfide, a novel gasotransmitter involved in gurad cell signaling. New Phytol 188:977–984. doi:10.1111/j.1469-8137.2010.03465.x

    Article  PubMed  Google Scholar 

  • González L, Bolaño C, Pellissier F (2003) Use of oxygen electrode in measurements of photosynthesis and respiration. In: Reigosa JMR (ed) Handbook of plant ecophysiology techniques. Springer, Netherlands, pp 141–153

    Chapter  Google Scholar 

  • Hou ZH, Wang LX, Liu J, Hou LX, Liu X (2013) Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J Integr Plant Biol 55(3):277–289. doi:10.1111/jipb.12004

    Article  CAS  PubMed  Google Scholar 

  • Huang XY, Chao DY, Gao JP et al (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817. doi:10.1101/gad.1812409

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Igamberdiev AU, Mikkelsen TN, Ambus P, Bauwe H, Lea Pj, Gardeström P (2004) Photorespiration contributes to stomatal regulation and carbon isotope fractionation: a study with barley, potato and Arabidopsis plants deficient in glycine decarboxylase. Photosynth Res 81:139–152. doi:10.1023/B:PRES.0000035026.05237.ec

    Article  CAS  Google Scholar 

  • Jin ZP, Shen JJ, Qiao ZJ, Yang GD, Wang R, Pei YX (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486. doi:10.1016/j.bbrc.2011.09.090

    Article  CAS  PubMed  Google Scholar 

  • Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46. doi:10.1016/j.plaphy.2012.10.017

    Article  CAS  PubMed  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349. doi:10.1146/annurev.pp.42.060191.001525

    Article  CAS  Google Scholar 

  • Ku SB, Edwards GE (1977) Oxygen inhibition of photosynthesis. I. temperature dependence and relation to O2/CO2 solubility ratio. Plant Physiol 59:986–990. doi:10.1104/pp.59.5.986

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li L, Bhatia M, Moore PK (2006) Hydrogen sulphide—a novel mediator of inflammation? Curr Opin Pharmacol 6:125–129. doi:10.1016/j.coph.2005.10.007

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36(8):1564–1572. doi:10.1111/pce.12092

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43(3):379–393. doi:10.1007/s11099-005-0062-6

    Article  CAS  Google Scholar 

  • Lilley RM, Walker DA (1975) Carbon dioxide assimilation by leaves, isolated chloroplasts, and ribulose bisphosphate carboxylase from Spinach. Plant Physiol 55:1087–1092. http://www.jstor.org/stable/4264081

  • Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935. doi:10.1016/j.plaphy.2010.09.016

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Wood ME, Whiteman M, Hancock JT (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signal Behav 6(10):1444–1446. doi:10.4161/psb.6.10.17104

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36(9):1607–1616. doi:10.1111/pce.12073

    Article  CAS  PubMed  Google Scholar 

  • Maherali H, Reid CD, Polley HW, Johnson HB, Jachson RB (2002) Stomatal acclimation over a subambient to elevated CO2 gradient in a C3/C4 grassland. Plant Cell Environ 25:557–566. doi:10.1046/j.1365-3040.2002.00832.x

    Article  CAS  Google Scholar 

  • Malone SR, Mayeux HS, Johnson HB, Wayne Polley H (1993) Stomatal density and aperture length in four plant species grown across a subambient CO2 gradient. Am J Bot 80:1413–1418. http://www.jstor.org/stable/2445670

  • Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16. doi:10.1104/pp.010707

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Niu SL, Jiang GM, Wan SQ, Li YG, Gao LM, Liu MZ (2006) A sand-fixing pioneer C3 species in sandland displays characteristics of C4 metabolism. Environ Exp Bot 57:123–130. doi:10.1016/j.envexpbot.2005.05.005

    Article  CAS  Google Scholar 

  • Offermann S, Okita TW, Edwards GE (2011) Resolving the compartmentation and function of C4 photosynthesis in the single-cell C4 species Bienertia sinuspersici. Plant Physiol 155:1612–1628. doi:10.1104/pp.110.170381

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Palavan-Unsal N, Arisan D (2009) Nitric oxide signalling in plants. Bot Rev 75:203–229. doi:10.1046/j.1469-8137.2003.00804.x

    Article  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants- from the field to the test tube and back. Plant Biol 9:582–588. doi:10.1055/s-2007-965424

    Article  CAS  PubMed  Google Scholar 

  • Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40(1):13–29. doi:10.1023/A:1020125719386

    Article  Google Scholar 

  • Sa ZS, Huang LQ, Wu GL, Ding JP, Chen XY, Yu T, Shi C, Shen WB (2007) Carbon monoxide: a novel antioxidant against oxidative stress in wheat seedling leaves. J Integr Plant Biol 49(5):638–645. doi:10.1111/j.1744-7909.2007.00461.x

    Article  CAS  Google Scholar 

  • Stimler K, Berry JA, Yakir D (2012) Effects of carbonyl sulfide and carbonic anhydrase on stomatal conductance. Plant Physiol 158:524–530. doi:10.1104/pp.111.185926

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sylvester AW, Parker-Clark V, Murray GA (2001) Leaf shape and anatomy as indicators of phase change in grasses: comparison of maize, rice, and bluegrass. Am J Bot 88(12):2157–2167

    Article  CAS  PubMed  Google Scholar 

  • Wang BL, Shi L, Li YX, Zhang WH (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231:1301–1309. doi:10.1007/s00425-010-1134-9

    Article  CAS  PubMed  Google Scholar 

  • Wang YQ, Li L, Cui WT, Xu S, Shen WB, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119. doi:10.1007/s11104-011-0936-2

    Article  CAS  Google Scholar 

  • Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327:617–618. doi:10.1038/327617a0

    Article  Google Scholar 

  • Xiao M, Ma J, Li HY, Jin H, Feng HQ (2010) Effects of hydrogen sulfide on alternative pathway respiration and induction of alternative oxidase gene expression in rice suspension cells. J Biosci 65(7–8):463–471

    CAS  Google Scholar 

  • Xu ZZ, Zhou GS (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59(12):3317–3325. doi:10.1093/jxb/ern185

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi K, Nishimura M (2000) Reduction to below threshold levels of glycolate oxidase activities in transgenic tobacco enhances photoinhibition during irradiation. Plant Cell Physiol 41(12):1397–1406. doi:10.1093/pcp/pcd074

    Article  CAS  PubMed  Google Scholar 

  • Ye ZP (2010) A review on modeling of responses of photosynthesis to light and CO2. Chin J Plant Ecol 34(6):727–740 [In Chinese]

    CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, Los Baños (Philippines), pp 61–64

    Google Scholar 

  • Yoshimura Y, Kubota F, Hirao K (2001) Estimation of photorespiration rate by simultaneous measurements of CO2, gas exchange rate, and chlorophyll fluorescence quenching in the C3 plant Vigna radiata (L.) Wilczek and the C4 plant Amaranthus mongostanus L. Photosynthetica 39(3):377–382. doi:10.1023/A:1015178209845

    Article  CAS  Google Scholar 

  • Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529. doi:10.1111/j.1744-7909.2008.00769.x

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094. doi:10.1111/j.1744-7909.2009.00885.x

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250. doi:10.1007/s10725-009-9372-1

    Article  CAS  Google Scholar 

  • Zhang H, Jiao H, Jiang CX, Wang SH, Wei ZJ, Luo JP, Jones RL (2010a) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 32:849–857. doi:10.1007/s11738-010-0469-y

    Article  CAS  Google Scholar 

  • Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010b) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567. doi:10.1111/j.1744-7909.2010.00946.x

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Life Sciences, Nanjing Agricultural University, Nanjing, China

    Bingbing Duan, Mengrou Jiang, Fei Yang, Lin Ni & Wei Lu

  2. College of Horticulture, Nanjing Agricultural University, Nanjing, China

    Yuehua Ma

Authors
  1. Bingbing Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuehua Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mengrou Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fei Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lin Ni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wei Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wei Lu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Duan, B., Ma, Y., Jiang, M. et al. Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment. Plant Growth Regul 75, 33–44 (2015). https://doi.org/10.1007/s10725-014-9929-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-014-9929-5

Keywords

Search

Navigation