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Soil inoculation with Burkholderia sp. LD-11 has positive effect on water-use efficiency in inbred lines of maize

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Abstract

Background and aims

Plant-growth promoting rhizobacteria (PGPR) can promote plant performance under water deficit, but the physiology and biochemistry of the promoting process induced by PGPR under different water deficits is not well known in maize (Zea mays L).

Methods

A glasshouse study was conducted to determine the effects of Burkholderia sp. LD-11 on morphophysiological traits for plant growth and homeostasis between reactive oxygen species (ROS) and antioxidant enzymes under five regimens in two maize inbred lines.

Results

Soil inoculation with Burkholderia sp. LD-11 promoted biomass accumulation and improved instantaneous water-use efficiency (WUEi), regardless of the soil water availability. It also triggered production of indole-3-acetic acid (IAA), decreasing the accumulation of abscisic acid (ABA) induced by the water deficit, alleviated ROS accumulation, and resulted in a reduction in lipid peroxidation induced by the water deficits. Soil inoculation also enhanced the tolerance to water deficit through reducing stomatal aperture by increasing the sensitivity of stomatal conductance (g s) to small changes in ABA concentration in the leaves.

Conclusions

Soil inoculation with Burkholderia sp. LD-11 enhanced root systems and WUEi, offering a potential avenue for improving maize tolerance to water deficit.

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Abbreviations

ABA:

Abscisic acid

ACC:

1-aminocyclopropane-1-carboxylic acid

CAT:

Catalase

g s :

Stomatal conductance

IAA:

Indole-3-acetic acid

LWP:

Leaf water potential

MDA:

Malondialdehyde

PFC:

Pot soil water capacity

PGPR:

Plant growth promoting rhizobacteria

Pn :

Net leaf photosynthetic rate

POD:

Peroxidase

PPFD:

Photosynthetic photon flux density

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

SWC:

Soil water content

Tr :

Transpiration rate

WUEi:

Instantaneous water-use efficiency

References

  • Aasamaa K, Sõber A, Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Funct Plant Biol 28(8):765–774

    Article  Google Scholar 

  • Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology, vol 105. Academic, New York, pp 121–126

    Google Scholar 

  • Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safranova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol 181:413–423

    Article  CAS  PubMed  Google Scholar 

  • Bharti N, Yadav D, Barnawal D, Maji D, Kalra A (2013) Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J Microbiol Biotechnol 29:379–387

    Article  CAS  PubMed  Google Scholar 

  • Blum A (1996) Crop responses to drought and the interpretation of adaptation. Plant Growth Regul 20:135–148

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bresson J, Varoquaux F, Bontpart T, Touraine B, Vile D (2013) The PGPR strain Phyllobacterium brassicacearum STM196 induces a reproductive delay and physiological changes that result in improved drought tolerance in Arabidopsis. New Phytol 200:558–569

    Article  CAS  PubMed  Google Scholar 

  • Çakir R (2004) Effect of water stress at different development stages on vegetative and reproductive growth of corn. Field Crop Res 89:1–16

    Article  Google Scholar 

  • Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Marè C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crop Res 105:1–14

    Article  Google Scholar 

  • Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J, Ross ARS, Kermode AR (2005) The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintainance of seed dormancy, moist-chilling and germination. Plant J 42:35–48

    Article  CAS  PubMed  Google Scholar 

  • Connor DJ, Palta JA (1981) The response of Cassava to water shortage. III stomatal control of plant water status. Field Crop Res 4:297–311

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fan XW, Li FM, Song L, Xiong YC, An LZ, Jia Y, Fang XW (2009) Defense strategy of old and modern spring wheat varieties during soil drying. Physiol Plant 136:310–323

    Article  CAS  PubMed  Google Scholar 

  • Franks PJ, Cowan IR, Farquhar GD (1997) The apparent feedforward response of stomata to air vapour pressure deficit: information revealed by different experimental procedures with two rainforest trees. Plant Cell Environ 20(1):142–145

    Article  Google Scholar 

  • Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Ann Rev Ecol Evol Syst 42:23–46

    Article  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312

    Article  CAS  PubMed  Google Scholar 

  • Hori K, Wada A, Shibuta T (1997) Changes in phenoloxidase activities of the galls on leaves of Ulmus vidana formed by Tetraneura funiformis (Homoptera: Eriosomatidae). Appl Entomol Zool 32:365–371

    CAS  Google Scholar 

  • Huang GH, Tian HH, Liu HY, Fan XW, Liang Y, Li YZ (2013) Characterization of plant-growth-promoting effects and concurrent promotion of heavy metal accumulation in the tissues of the plants grown in the polluted soil by Burkholderia Strain LD-11. Int J Phytoremediation 15:991–1009

    Article  CAS  PubMed  Google Scholar 

  • Jiang F, Hartung W (2008) Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. J Exp Bot 59:37–43

    Article  CAS  PubMed  Google Scholar 

  • Kandeler E, Marschner P, Tscherko D, Gahoonia TS, Nielsen NE (2002) Microbial community composition and functional diversity in the rhizosphere of maize. Plant Soil 238:301–312

    Article  CAS  Google Scholar 

  • Kobata T, Palta JA, Turner NC (1992) Rate of development of post-anthesis water deficits and grain filling of spring wheat. Crop Sci 32:1238–1242

    Article  Google Scholar 

  • Lalande R, Bissonnette N, Coutlée D, Antoun H (1989) Identification of rhizobacteria from maize and determination of their plant-growth promoting potential. Plant Soil 115:7–11

    Article  Google Scholar 

  • Li YZ, Sun CB, Huang ZB, Pan JL, Wang L, Fan XW (2009) Mechanisms of progressive water deficit tolerance and growth recovery of Chinese maize foundation genotypes Huangzao 4 and Chang 7–2, which are proposed on the basis of comparison of physiological and transcriptomic responses. Plant Cell Physiol 50:2092–2111

    Article  CAS  PubMed  Google Scholar 

  • Liu FC, Xing SJ, Ma HL, Du ZY, Ma BY (2013) Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 97:9155–9164

    Article  CAS  PubMed  Google Scholar 

  • Lopez M, Tejera NA, Iribarne C, Lluch C, Herrera-Cervera JA (2008) Trehalose and trehalase in root nodules of Medicago truncatula and Phaseolus vulgaris in response to salt stress. Physiol Plant 134:575–582

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  PubMed  Google Scholar 

  • Luna CM, Pastori GM, Driscoll S, Groten K, Bernard S, Foyer CH (2005) Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. J Exp Bot 56:417–423

    Article  CAS  PubMed  Google Scholar 

  • Maiti RK, Maiti LE, Maiti S, Maiti AM, Maiti M, Maiti H (1996) Genotypic variability in maize cultivars (Zea mays L.) for resistance to drought and salinity at the seedling stage. J Plant Physiol 148:741–744

    Article  CAS  Google Scholar 

  • Martínez EM, Rey BJ, Fandiño M, Cancela JJ (2013) Comparison of two techniques for measuring leaf water potential in Vitis Vinifera Var. Albarino. Ciência Téc Vitiv 28(1):29–41

    Google Scholar 

  • Marulanda A, Barea JM, Azcon R (2006) An indigenous drought-tolerant strain of Glomus intraradices associated with a native bacterium improves water-transport and root development in Retama sphaerocarpa. Microb Ecol 52:670–678

    Article  CAS  PubMed  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomato and pepper. Plant Sci 166:525–530

    Article  CAS  Google Scholar 

  • Mencuccini M, Mambelli S, Comstock J (2000) Stomatal responsiveness to leaf water status in common bean (Phaseolus vulgaris L.) is a function of time of day. Plant Cell Environ 23(10):1109–1118

    Article  Google Scholar 

  • Mwange KN, Hou HW, Cui KM (2003) Relationship between endogenous indole-3-acetic acid and abscisic acid changes and bark recovery in Eucommia ulmoides Oliv after girdling. J Exp Bot 54:1899–1907

    Article  CAS  PubMed  Google Scholar 

  • Naveed M, Mitter B, Reichenauer TG, Wieczorekc K, Sessitsch A (2014) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans Ps JN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39

    Article  CAS  Google Scholar 

  • Palta JA, Watt M (2009) Crop roots systems form and function: improving the capture of water and nutrients with vigorous root systems. In: Sadras V, Calderini D (eds) Crop physiology: applications for genetic improvement and agronomy. Academic, San Diego, pp 309–325

    Chapter  Google Scholar 

  • Palta JA, Chen X, Milroy SP, Rebetzke GJ, Dreccer MF, Watt M (2011) Large root systems: are they useful in adapting wheat to dry environments? Funct Plant Biol 38:347–354

    Article  Google Scholar 

  • Patten CL, Glick BR (2002) Role of pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Penrose DM, Glick BR (2001) Levels of ACC and related compounds in exudates and extracts of canola seeds treated with ACC-deaminase-containing plant growth promoting bacteria. Can J Micobiol 47:368–372

    Article  CAS  Google Scholar 

  • Pérez-Montaño F, Alías-Villegas C, Bellogín RA, del Cerro P, Espuny MR, Jiménez-Guerrero I, López-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336

    Article  PubMed  Google Scholar 

  • Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Cei FP, Borin S, Sorlini C, Zocchi G, Daffonchio D (2014) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol. doi:10.1111/1462-2920.12439

    PubMed  Google Scholar 

  • Ryan A, Cojocariu C, Possell M, Davies WJ, Hewitt CN (2009) Defining hybrid poplar (Populus deltoides x Populus trichocarpa) tolerance to ozone: identifying key parameters. Plant Cell Environ 32:31–45

    Article  CAS  PubMed  Google Scholar 

  • Sinclair TR, BENNET JM, Muchow RC (1990) Relative sensitivity of grain yield and biomass accumulation to drought in field grown maize. Crop Sci 30:690–693

    Article  Google Scholar 

  • Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51(350):1531–1542

    Article  CAS  PubMed  Google Scholar 

  • Tubiello FN, Amthor JA, Boote K, Donatelli M, Easterling WE, Fisher G, Gifford R, Howden M, Reilly J, Rosenzweig C (2007) Crop response to elevated CO2 and world food supply. Eur J Agron 26:215–228

    Article  CAS  Google Scholar 

  • Vardharajula S, Ali SZ, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus sp: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6:1–14

    Article  CAS  Google Scholar 

  • Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2 that overproduce indoleacetic acid. Curr Microbiol 32:67–71

    Article  CAS  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Dashti N, Hynes RK, Smith DL (1997) Plant growth-promoting rhizobacteria and soybean [Glycine max (L.) Merr.] growth and physiology at suboptimal root zone temperatures. Ann Bot 79(3):243–249

    Article  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 

  • Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Paré PW (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant Microbe Interact 23(8):1097–1104

    Article  CAS  PubMed  Google Scholar 

  • Zhao SJ, Xu C, Zou Q, Meng Q (1994) Improvements of method for measurement of malondialdehyde in plant tissues. Plant Physiol Commun 30:207–210 (in chinese)

    CAS  Google Scholar 

  • Zolla G, Badri DV, Bakker MG, Manter DK, Vivanco JM (2013) Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl Soil Ecol 68:1–9

    Article  Google Scholar 

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Acknowledgments

The authors appreciate three anonymous referees for their valuable comments. We are also thankful to Dr. Yanlei Du for his comments on the manuscript and Mr. Dengfeng Dong for his experimental assistance. This research was supported by the NSFC project (31160287, 31360337), Guangxi Natural Science Foundation (2014GXNSFAA118098), and Project of the Special Basic Work of Ministry (2014FY120100).

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Correspondence to Xianwei Fan.

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Responsible Editor: Jesus Mercado-Blanco.

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Fan, X., Hu, H., Huang, G. et al. Soil inoculation with Burkholderia sp. LD-11 has positive effect on water-use efficiency in inbred lines of maize. Plant Soil 390, 337–349 (2015). https://doi.org/10.1007/s11104-015-2410-z

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