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Research paper | Open Access

Piriformospora indica confers drought tolerance on Zea mays L. through enhancement of antioxidant activity and expression of drought-related genes

Le Xu1, Aiai Wang1, Jun Wang, Qiao Wei, Wenying Zhang( )
Hubei Collaborative Innovation Center for Grain Industry/Research Center of Crop Stresses Resistance Technologies, Yangtze University, Jingzhou 434025, China

1 These authors contributed equally to this work.

Peer review under responsibility of Crop Science Society of China and Institute of Crop Science, CAAS.

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Abstract

Drought stress is one of the most severe environmental constraints to plant growth and crop productivity. Plant growth is greatly affected by drought stress, and plants, to survive, adapt to this stress by invoking different pathways. Piriformospora indica, a root-colonizing endophytic fungus of Sebacinales, promotes plant growth and confers resistance to biotic and abiotic stresses, including drought stress, by affecting the physiological properties of the host plant. The fungus strongly colonizes the roots of maize (Zea mays L.) and promotes shoot and root growth under both normal growth conditions and drought stress. We used polyethylene glycol (PEG-6000) to mimic drought stress and found that root fresh and dry weight, leaf area, SPAD value, and leaf number were increased in P. indica-colonized plants. The antioxidative activities of catalases and superoxide dismutases were upregulated within 24h in the leaves of P. indica-colonized plants. Drought-related genes DREB2A, CBL1, ANAC072, and RD29A were upregulated in drought-stressed leaves of P. indica-colonized plants. Furthermore, after drought treatment, proline content increased, whereas accumulation of malondialdehyde (MDA), an indicator of membrane damage, decreased in P. indica-colonized maize. We conclude that P. indica-mediated plant protection against the detrimental effects of drought may result from enhanced antioxidant enzyme activity, proline accumulation, and expression of drought-related genes and lower membrane damage in maize plants.

Keywords

AntioxidantsDrought-related genesDrought tolerancePiriformospora indicaMaize

References

[1]

M. Khayatnezhad, M. Hasanuzzaman, R. Gholamin, Assessment of yield and yield components and drought tolerance at end-of season drought condition on corn hybrids (Zea mays L.), Aust. J. Crop. Sci. 5 (2015) 1493–1500.
Google Scholar
[2]

M.S. Lopes, J.L. Araus, P.D. van Heerden, C.H. Foyer, Enhancing drought tolerance in C crops, J. Exp. Bot. 62 (2011) 3135–3153.
Crossref Google Scholar
[3]

S. Verma, A. Varma, K.H. Rexer, A. Hassel, G. Kost, A. Sarbhoy, P. Bisen, B. Bütehorn, P. Franken, Piriformospora indica, gen. et sp. nov, a new root-colonizing fungus, Mycologia 90 (1998) 896–903.
Crossref Google Scholar
[4]

R. Oelmüller, I. Sherameti, S. Tripathi, A. Varma, Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications, Symbiosis 49 (2009) 1–17.
Crossref Google Scholar
[5]

A. Varma, S. Verma, Sudha, N. Sahay, B. Bütehorn, P. Franken, Piriformospora indica, a cultivable plant-growth-promoting root endophyte, Appl. Environ. Microbiol. 65 (1999) 2741–2744.
Crossref Google Scholar
[6]

K. Apel, H. Hirt, Reactive oxygen species, metabolism, oxidative stress, and signal transduction, Annu. Rev. Plant Biol. 55 (2004) 373–399.
Crossref Google Scholar
[7]

R. Mittler, S. Vanderauwera, M. Gollery, F. Van Breusegem, Reactive oxygen gene network of plants, Trends Plant Sci. 9 (2004) 490–498.
Crossref Google Scholar
[8]

R. Sairam, G. Srivastava, S. Agarwal, R. Meena, Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes, Biol. Plant. 49 (2005) 85–91.
Crossref Google Scholar
[9]

V. Shulaev, Metabolomics technology and bioinformatics, Brief. Bioinform. 7 (2006) 128–139.
Crossref Google Scholar
[10]

C.H. Foyer, G. Noctor, Oxygen processing in photosynthesis, regulation and signaling, New Phytol. 146 (2000) 359–388.
Crossref Google Scholar
[11]

C. Sun, J.M. Johnson, D.G. Cai, I. Sherameti, R. Oelmuller, B.G. Lou, Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein, J. Plant Physiol. 16712 (2010) 1009–1017.
Crossref Google Scholar
[12]

I. Sherameti, Y. Venus, C. Drzewiecki, S. Tripathi, V.M. Dan, I. Nitz, A. Varma, F.M. Grundler, R. Oelmüller, PYK10, a β-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica, Plant J. 54 (2008) 428–439.
Crossref Google Scholar
[13]

G. Ghanem, A. Ewald, S. Zerche, F. Hennig, Effect of root colonization with Piriformospora indica and phosphate availability on the growth and reproductive biology of a Cyclamen persicum cultivar, Sci. Hortic. 172 (2014) 233–241.
Crossref Google Scholar
[14]

L. Bækgaard, L. Luoni, M.I. De Michelis, M.G. Palmgren, The plant plasma membrane Ca2+ pump ACA8 contains overlapping as well as physically separated autoinhibitory and calmodulin-binding domains, J. Biol. Chem. 281 (2006) 1058–1065.
Crossref Google Scholar
[15]

C.N. Giannopolitis, S.K. Ries, Superoxide dismutases: I. Occurrence in higher plants, Plant Physiol. 59 (1977) 309–314.
Crossref Google Scholar
[16]

T.E. Kraus, R.A. Fletcher, Paclobutrazol protects wheat seedlings from heat and paraquat injury. Is detoxification of active oxygen involved? Plant Cell Physiol. 35 (1994) 45–52.
Google Scholar
[17]

I. Cakmak, H. Marschner, Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves, Plant Physiol. 98 (1992) 1222–1227.
Crossref Google Scholar
[18]

D.M. Hodges, J.M. DeLong, C.F. Forney, R.K. Prange, Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds, Planta 207 (1999) 604–611.
Crossref Google Scholar
[19]

M. Ashraf, M. Foolad, Roles of glycine betaine and proline in improving plant abiotic stress resistance, Environ. Exp. Bot. 59 (2007) 206–216.
Crossref Google Scholar
[20]

D. Del Rio, A.J. Stewart, N. Pellegrini, A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress, Nutr. Metab. Cardiovas. 15 (2005) 316–328.
Crossref Google Scholar
[21]

W.A. Pryor, J. Stanley, Suggested mechanism for the production of malonaldehyde during the autoxidation of polyunsaturated fatty acids. Nonenzymic production of prostaglandin endoperoxides during autoxidation, J. Org. Chem. 40 (1975) 3615–3617.
Crossref Google Scholar
[22]

H. Baltruschat, J. Fodor, B.D. Harrach, E. Niemczyk, B. Barna, G. Gullner, A. Janeczko, K.H. Kogel, P. Schäfer, I. Schwarczinger, Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants, New Phytol. 180 (2008) 501–510.
Crossref Google Scholar
[23]

J. Vadassery, S. Ranf, C. Drzewiecki, A. Mithöfer, C. Mazars, D. Scheel, J. Lee, R. Oelmüller, A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots, Plant J. 59 (2009) 193–206.
Crossref Google Scholar
[24]

L.S. Phan Tran, K. Nakashima, Y. Sakuma, S.D. Simpson, Y. Fujita, K. Maruyama, M. Fujita, M. Seki, K. Shinozaki, K. Yamaguchi-Shinozaki, Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter, Plant Cell 16 (2004) 2481–2498.
Crossref Google Scholar
[25]

Y. Sakuma, Q. Liu, J.G. Dubouzet, H. Abe, K. Shinozaki, K. Yamaguchi-Shinozaki, DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression, Biochem. Biophys. Res. Commun. 290 (2002) 998–1009.
Crossref Google Scholar
[26]

Y.Y. Zhang, C.W. Yang, Y. Li, N.Y. Zheng, H. Chen, Q.Z. Zhao, T. Gao, H.S. Guo, Q. Xie, SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis, Plant Cell 19 (2007) 1912–1929.
Crossref Google Scholar
[27]

P.D. Moore, Proline implicated in halophyte osmotic adjustment, Nature 253 (1975) 399–400.
Crossref Google Scholar
[28]

M.J. Zarea, S. Hajinia, N. Karimi, E.M. Goltapeh, F. Rejali, A. Varma, Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl, Soil Biol. Biochem. 45 (2011) 139–146.
Crossref Google Scholar
[29]

F. Waller, B. Achatz, H. Baltruschat, J. Fodor, K. Becker, M. Fischer, T. Heier, R. Hückelhoven, C. Neumann, D. von Wettstein, The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield, Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 13386–13391.
Crossref Google Scholar
[30]

C.H. Foyer, S. Shigeoka, Understanding oxidative stress and antioxidant functions to enhance photosynthesis, Plant Physiol. 300 (2011) 429–434.
Google Scholar
[31]

J.F. White, M.S. Torres, Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol. Plant. 138 (2010) 440–446.
Crossref Google Scholar
[32]

C.E. Hamilton, P.E. Gundel, M. Helander, K. Saikkonen, Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review, Fungal Divers. 54 (2011) 1–10.
Crossref Google Scholar
[33]

Y. Yaghoubian, E.M. Goltapeh, H. Pirdashti, E. Esfandiari, V. Feiziasl, H.K. Dolatabadi, A. Varma, M.H. Hassim, Effect of Glomus mosseae and Piriformospora indica on growth and antioxidant defense responses of wheat plants under drought stress, Agric. Res. 3 (2014) 239–245.
Crossref Google Scholar
[34]

N.C. Gassner, C.M. Tamble, J.E. Bock, N. Cotton, K.N. White, K. Tenney, R.P. St. Onge, M.J. Proctor, G. Giaever, C. Nislow, Accelerating the discovery of biologically active small molecules using a high-throughput yeast halo assay, J. Nat. Prod. 70 (2007) 383–390.
Crossref Google Scholar
[35]

F.C. Peterson, E.S. Burgie, S.Y. Park, D.R. Jensen, J.J. Weiner, C.A. Bingman, C.E.A. Chang, S.R. Cutler,, B.F. Volkman, Structural basis for selective activation of ABA receptors, Nat. Struct. Mol. Biol. 17 (2010) 1109–1113.
Crossref Google Scholar
[36]

A. Mosquna, F.C. Peterson, S.Y. Park, J. Lozano-Juste, B.F. Volkman, S.R. Cutler, Potent and selective activation of abscisic acid receptors in vivo by mutational stabilization of their agonist-bound conformation, Proc. Natl. Acad. Sci. U. S. A. 108 (2011) 20838–20843.
Crossref Google Scholar
[37]

T. Peskan-Berghöfer, A. Vilches-Barro, T.M. Müller, E. Glawischnig, M. Reichelt, J. Gershenzon, T. Rausch, Sustained exposure to abscisic acid enhances the colonization potential of the mutualist fungus Piriformospora indica on Arabidopsis thaliana roots, New Phytol. 208 (2015) 873–886.
Crossref Google Scholar
[38]

P. Ohri, R. Bhardwaj, S. Bali, R. Kaur, S. Jasrotia, A. Khajuria, R.D. Parihar, The common molecular players in plant hormone crosstalk and signaling, Curr. Protein Pept. Sci. 16 (2015) 369–388.
Crossref Google Scholar
The Crop Journal
Volume 5 Issue 3,
June 2017
Pages 251-258
DOI: 10.1016/j.cj.2016.10.002
Cite this article:
Xu L, Wang A, Wang J, et al. Piriformospora indica confers drought tolerance on Zea mays L. through enhancement of antioxidant activity and expression of drought-related genes. The Crop Journal, 2017, 5(3): 251-258. https://doi.org/10.1016/j.cj.2016.10.002

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Received: 20 May 2016
Revised: 13 September 2016
Accepted: 02 November 2016
Published: 12 November 2016
© 2016 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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