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Bacillus subtilis-regulation of stomatal movement and instantaneous water use efficiency in Vicia faba

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Abstract

Microbes- and microbe-associated molecular patterns-induced stomatal closure have been known to be connected with the early defense responses and the improvement of instantaneous water use efficiency (WUEi) in plants. Being a commercially available microorganism, Bacillus subtilis can promote plant growth and induce disease resistance. However, its effects on stomatal movement and WUEi in plants have been largely unexplored. Here, we showed that B. subtilis induced stomatal closure in a dose- and time-dependent manner when applied to isolated epidermal peels and intact leaves of broad bean. Pharmacological study further revealed that the B. subtilis-induced stomatal closure in epidermal peels was mediated mainly by reactive oxygen species production via NADPH oxidases. Furthermore, foliar application of B. subtilis significantly reduced stomatal aperture, stomatal conductance (gs), transpiration rate (E) and net photosynthesis rate (Pn) of leaves of broad bean at 8 and 24 h, reductions in which were reversed after 48 h. As a consequence, the WUEi of plants treated with B. subtilis for 8–144 h was higher than that in the control. The chlorophyll fluorescence and content analysis further demonstrated that B. subtilis could enhance plant photosynthetic activities by increasing leaf photosynthetic efficiency and chlorophyll content. These results suggest that foliar spray of B. subtilis can improve WUEi of crop plant via the regulations of stomatal movement and photosynthetic activity during a special time period.

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Abbreviations

CAT:

Catalase

Ci :

Intercellular CO2 concentration

DPI:

Diphenylene iodonium chloride

E:

Transpiration rate

Fv/Fm:

Maximum quantum yield of photosystem II (PSII)

gs :

Stomatal conductance

NPQ:

Non-photochemical quenching

Pn :

Net photosynthetic rate

ΦPSII:

Effective quantum yield of PSII

qP:

Photochemical quenching

ROS:

Reactive oxygen species

SHAM:

Salicylhydroxamic acid

WUEi :

Instantaneous water use efficiency

References

  • Acharya BR, Assmann SM (2009) Hormone interactions in stomatal function. Plant Mol Biol 69:451–462

    Article  CAS  PubMed  Google Scholar 

  • Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaves M, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Dodd IC, Davies WJ, Wilkinson S (2013) Ethylene limits abscisic acid- or soil drying-induced stomatal closure in aged wheat leaves. Plant, Cell Environ 36:1850–1859

    Article  CAS  Google Scholar 

  • Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88

    Article  CAS  PubMed  Google Scholar 

  • Cuevas JC, Sánchez DH, Marina M, Ruiz OA (2004) Do polyamines modulate the Lotus glaber NADPH oxidation activity induced by the herbicide methyl viologen? Funct Plant Biol 31:921–928

    Article  CAS  Google Scholar 

  • Davies WJ, Wilkinson S, Loveys B (2002) Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytol 153:449–460

    Article  CAS  Google Scholar 

  • Deng B, Jin X, Yang Y, Lin Z, Zhang Y (2014) The regulatory role of riboflavin in the drought tolerance of tobacco plants depends on ROS production. Plant Growth Regul 72:269–277

    Article  CAS  Google Scholar 

  • Desikan R, Cheung MK, Clarke A, Golding S, Sagi M, Fluhr R et al (2004) Hydrogen peroxide is a common signal for darkness-and ABA-induced stomatal closure in Pisum sativum. Funct Plant Biol 31:913–920

    Article  CAS  Google Scholar 

  • Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R et al (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47:907–916

    Article  CAS  PubMed  Google Scholar 

  • Farquhar G, Richards R (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Funct Plant Biol 11:539–552

    CAS  Google Scholar 

  • Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao J, Wang N, Wang G-X (2013) Saccharomyces cerevisiae-induced stomatal closure mainly mediated by salicylhydroxamic acid-sensitive peroxidases in Vicia faba. Plant Physiol Biochem 65:27–31

    Article  CAS  PubMed  Google Scholar 

  • Grimmer MK, Foulkes MJ, Paveley ND (2012) Foliar pathogenesis and plant water relations: a review. J Exp Bot 63:4321–4331

    Article  CAS  PubMed  Google Scholar 

  • He J, Yue X, Wang R, Zhang Y (2011) Ethylene mediates UV-B-induced stomatal closure via peroxidase-dependent hydrogen peroxide synthesis in Vicia faba L. J Exp Bot 62:2657–2666

    Article  CAS  PubMed  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  CAS  PubMed  Google Scholar 

  • Hoque TS, Uraji M, Ye W, Hossain MA, Nakamura Y, Murata Y (2012) Methylglyoxal-induced stomatal closure accompanied by peroxidase-mediated ROS production in Arabidopsis. J Plant Physiol 169:979–986

    Article  CAS  PubMed  Google Scholar 

  • Hunsche M, Bürling K, Saied A, Schmitz-Eiberger M, Sohail M, Gebauer J, Noga G, Buerkert A (2010) Effects of NaCl on surface properties, chlorophyll fluorescence and light remission, and cellular compounds of Grewia tenax (Forssk.) Fiori and Tamarindus indica L. leaves. Plant Growth Regul 61:253–263

    Article  CAS  Google Scholar 

  • Iriti M, Picchi V, Rossoni M, Gomarasca S, Ludwig N, Gargano M et al (2009) Chitosan antitranspirant activity is due to abscisic acid-dependent stomatal closure. Environ Exp Bot 66:493–500

    Article  CAS  Google Scholar 

  • Joo JH, Wang S, Chen J, Jones A, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein α and β subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jourdan E, Henry G, Duby F, Dommes J, Barthelemy JP, Thonart P et al (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol Plant Microbe Interact 22:456–468

    Article  CAS  PubMed  Google Scholar 

  • Kautz B, Noga G, Hunsche M (2014) Sensing drought- and salinity-imposed stresses on tomato leaves by means of fluorescence techniques. Plant Growth Regul 73:279–288

    Article  CAS  Google Scholar 

  • Kerstiens G, Tych W, Robinson MF, Mansfield TA (2002) Sodium-related partial stomatal closure and salt tolerance of Aster tripolium. New Phytol 153:509–515

    Article  CAS  Google Scholar 

  • Khokon MAR, Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC et al (2010a) Yeast elicitor-induced stomatal closure and peroxidase-mediated ROS production in Arabidopsis. Plant Cell Physiol 51:1915–1921

    Article  CAS  PubMed  Google Scholar 

  • Khokon MAR, Uraji M, Munemasa S, Okuma E, Nakamura Y, Mori IC et al (2010b) Chitosan-induced stomatal closure accompanied by peroxidase-mediated reactive oxygen species production in Arabidopsis. Biosci Biotech Biochem 74:2313–2315

    Article  CAS  Google Scholar 

  • Khokon M, Jahan MS, Rahman T, Hossain MA, Muroyama D, Minami I et al (2011a) Allyl isothiocyanate (AITC) induces stomatal closure in Arabidopsis. Plant, Cell Environ 34:1900–1906

    Article  CAS  Google Scholar 

  • Khokon MAR, Okuma E, Hossain MA, Munemasa S, Uraji M, Nakamura Y et al (2011b) Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant, Cell Environ 34:434–443

    Article  CAS  Google Scholar 

  • Koers S, Guzel-Deger A, Marten I, Roelfsema MRG (2011) Barley mildew and its elicitor chitosan promote closed stomata by stimulating guard-cell S-type anion channels. Plant J 68:670–680

    Article  CAS  PubMed  Google Scholar 

  • Kumar AS, Lakshmanan V, Caplan JL, Powell D, Czymmek KJ, Levia DF et al (2012) Rhizobacteria Bacillus subtilis restricts foliar pathogen entry through stomata. Plant J 72:694–706

    Article  CAS  PubMed  Google Scholar 

  • Lawlor D, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell Environ 25:275–294

    Article  CAS  Google Scholar 

  • Li B, Yang Y, Yu C, Li S, Chen J, Liu X, Qin H, Wang D (2014a) Partial suppression of l-galactono-1,4-lactone dehydrogenase causes significant reduction in leaf water loss through decreasing stomatal aperture size in Arabidopsis. Plant Growth Regul 72:171–179

    Article  CAS  Google Scholar 

  • Li Y, Xu S-S, Gao J, Pan S, Wang G-X (2014b) Chlorella induces stomatal closure via NADPH oxidase-dependent ROS production and its effects on instantaneous water use efficiency in Vicia faba. PLoS One 9:e93290

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Liu F, Jensen CR, Shahanzari A, Andersen MN, Jacobsen SE (2005) ABA regulated stomatal control and photosynthetic water use efficiency of potato (Solanum tuberosum L.) during progressive soil drying. Plant Sci 168:831–836

    Article  CAS  Google Scholar 

  • Luis A, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272

    Article  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mori IC, Pinontoan R, Kawano T, Muto S (2001) Involvement of superoxide generation in salicylic acid-induced stomatal closure in Vicia faba. Plant Cell Physiol 42:1383–1388

    Article  CAS  PubMed  Google Scholar 

  • Mott KA (2009) Opinion: stomatal responses to light and CO2 depend on the mesophyll. Plant, Cell Environ 32:1479–1486

    Article  CAS  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD (P) H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nejad AR, van Meeteren U (2008) Dynamics of adaptation of stomatal behaviour to moderate or high relative air humidity in Tradescantia virginiana. J Exp Bot 59:289–301

    Article  Google Scholar 

  • Ongena M, Duby F, Jourdan E, Beaudry T, Jadin V, Dommes J et al (2005) Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl Microbiol Biot 67:692–698

    Article  CAS  Google Scholar 

  • Ongena M, Jourdan E, Adam A, Paquot M, Brans A, Joris B et al (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9:1084–1090

    Article  CAS  PubMed  Google Scholar 

  • Pérez-García A, Romero D, De Vicente A (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotech 22:187–193

    Article  PubMed  Google Scholar 

  • Rivero RM, Shulaev V, Blumwald E (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol 150:1530–1540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawinski K, Mersmann S, Robatzek S, Böhmer M (2013) Guarding the Green: pathways to stomatal immunity. Mol Plant-Microbe Interact 26:626–632

    Article  CAS  PubMed  Google Scholar 

  • Signarbieux C, Feller U (2011) Non-stomatal limitations of photosynthesis in grassland species under artificial drought in the field. Environ Exp Bot 71:192–197

    Article  CAS  Google Scholar 

  • Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate-and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trejo CL, Davies WJ, Ruiz L (1993) Sensitivity of stomata to abscisic acid (an effect of the mesophyll). Plant Physiol 102:497–502

    CAS  PubMed  PubMed Central  Google Scholar 

  • Underwood W, Melotto M, He SY (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9:1621–1629

    Article  CAS  PubMed  Google Scholar 

  • Vranova E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    Article  CAS  PubMed  Google Scholar 

  • Yu D, Kim S, Lee H (2009) Stomatal and non-stomatal limitations to photosynthesis in field-grown grapevine cultivars. Biol Plantarum 53:133–137

    Article  CAS  Google Scholar 

  • Zeng W, He SY (2010) A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol 153:1188–1198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work is supported by the National High-Tech R & D Program (863 Program) for the 12th Five-Year Plan (2011AA100503), Natural Science Fund of China (31330010) and Zhejiang Provincial Natural Science Foundation of China(LZ13C030002).

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Correspondence to Genxuan Wang.

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Li, Y., Xu, S., Gao, J. et al. Bacillus subtilis-regulation of stomatal movement and instantaneous water use efficiency in Vicia faba . Plant Growth Regul 78, 43–55 (2016). https://doi.org/10.1007/s10725-015-0073-7

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  • DOI: https://doi.org/10.1007/s10725-015-0073-7

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