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RESEARCH ARTICLE

Effect of endophytic fungus Piriformospora indica on yield and some physiological traits of millet (Panicum miliaceum) under water stress

Goudarz Ahmadvand A B and Somayeh Hajinia A
+ Author Affiliations
- Author Affiliations

A Department of Agronomy and Plant Breeding, College of Agriculture, Bu-Ali Sina University, Hamedan, Iran.

B Corresponding author. Email: gahmadvand@basu.ac.ir

Crop and Pasture Science 69(6) 594-605 https://doi.org/10.1071/CP17364
Submitted: 31 October 2017  Accepted: 23 March 2018   Published: 12 May 2018

Abstract

Piriformospora indica is one of the cultivable root-colonising endophytic fungi of the order Sebacinales, which efficiently promote plant growth, uptake of nutrients, and resistance to biotic and abiotic stresses. The aim of this study was to evaluate the effect of P. indica on millet (Panicum miliaceum L.) under water-stress conditions. Two field experiments were carried out in a factorial arrangement at Bu-Ali Sina University of Hamedan, Iran, during 2014 and 2015. The first factor was three levels of water-deficit stress, with irrigation after 60 mm (well-watered), 90 mm (mild stress) and 120 mm (severe stress) evaporation from pan class A. The second factor was two levels of fungus P. indica: inoculated and uninoculated. Results showed that water-deficit stress significantly decreased grain yield and yield components. Colonisation by P. indica significantly increased number of panicles per plant, number of grains per panicle and 1000-grain weight, regardless of water supply. Inoculation with P. indica increased grain yield by 11.4% (year 1) and 19.72% (year 2) in well-watered conditions and by 35.34% (year 1) and 32.59% (year 2) under drought stress, compared with uninoculated plants. Maximum flag-leaf area (21.71 cm2) was achieved with well-watered conditions. Severe water stress decreased flag-leaf area by 53.36%. Flag-leaf area was increased by 18.64% by fungus inoculation compared with the uninoculated control. Under drought conditions, inoculation with P. indica increased plant height by 27.07% and panicle length by 9.61%. Severe water stress caused a significant decrease in grain phosphorus concentration, by 42.42%, compared with the well-watered treatment. By contrast, grain nitrogen and protein contents were increased about 30.23% and 30.18%, respectively, with severe water stress. Inoculation with P. indica increased grain phosphorus by 24.22%, nitrogen by 7.47% and protein content by 7.54% compared with control. Water stress reduced leaf chlorophyll and carotenoid concentrations, whereas P. indica inoculation enhanced chlorophyll concentrations by 27.18% under severe water stress. The results indicated the positive effect of P. indica on yield and physiological traits of millet in both well-watered and water-stressed conditions.

Additional keywords: abiotic stress, pigments, soil fungi, symbiosis.


References

Achatz B, von Rüden S, Andrade D, Neumann E, Pons-Kühnemann J, Kogel K-H, Franken P, Waller F (2010) Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant and Soil 333, 59–70.
Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development.Crossref | GoogleScholarGoogle Scholar |

Allen RG, Pereira LS, Raes D, Smith M (1998) ‘Crop evapotranspiration—Guidelines for computing crop water requirements.’ FAO Irrigation and Drainage Paper No. 56. (Food and Agriculture Organization of the United Nations: Rome)

Anith K, Faseela K, Archana P, Prathapan K (2011) Compatibility of Piriformospora indica and Trichoderma harzianum as dual inoculants in black pepper (Piper nigrum L.). Symbiosis 55, 11–17.
Compatibility of Piriformospora indica and Trichoderma harzianum as dual inoculants in black pepper (Piper nigrum L.).Crossref | GoogleScholarGoogle Scholar |

Anon. (1987) ‘Approved methods of the AACC. Method 11-46.’ (American Association of Cereal Chemists Inc.: St. Paul, MN, USA)

Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar |

Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 3–42.
Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar |

Barazani O, Benderoth M, Groten K, Kuhlemeier C, Baldwin IT (2005) Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata. Oecologia 146, 234–243.
Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata.Crossref | GoogleScholarGoogle Scholar |

Bradford KJ (1994) Water stress and the water relations of seed development: a critical review. Crop Science 34, 1–11.
Water stress and the water relations of seed development: a critical review.Crossref | GoogleScholarGoogle Scholar |

Celebi SZ, Demir S, Celebi R, Durak ED, Yilmaz IH (2010) The effect of Arbuscular Mycorrhizal Fungi (AMF) applications on the silage maize (Zea mays L.) yield in different irrigation regimes. European Journal of Soil Biology 46, 302–305.
The effect of Arbuscular Mycorrhizal Fungi (AMF) applications on the silage maize (Zea mays L.) yield in different irrigation regimes.Crossref | GoogleScholarGoogle Scholar |

Choudhury AK, Karim MA, Haque MM, Khaliq QA, Ahmed JU, Hossain MM (2011) Genotypic variability in plant water status of French bean under drought stress. Journal of Crop Science and Biotechnology 14, 17–24.
Genotypic variability in plant water status of French bean under drought stress.Crossref | GoogleScholarGoogle Scholar |

Diouf O, Brou Y, Diouf M, Sarr B, Eyletters M, Roy-Macauley H, Delhaye J (2004) Response of pearl millet to nitrogen as affected by water deficit. Agronomie 24, 77–84.
Response of pearl millet to nitrogen as affected by water deficit.Crossref | GoogleScholarGoogle Scholar |

Doorenbos J, Pruitt W (1992) Calculation of crop water requirement. In ‘Crop water requirement’. (Food and Agriculture Organization of the United Nations: Rome)

Fabbrin EG, Gogorcena Y, Mogor AF, Garmendia I, Goicoechea N (2015) Pearl millet growth and biochemical alterations determined by mycorrhizal inoculation, water availability and atmospheric CO2 concentration. Crop & Pasture Science 66, 831–840.
Pearl millet growth and biochemical alterations determined by mycorrhizal inoculation, water availability and atmospheric CO2 concentration.Crossref | GoogleScholarGoogle Scholar |

Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S (2009) Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development 29, 185–212.
Plant drought stress: effects, mechanisms and management.Crossref | GoogleScholarGoogle Scholar |

Franken P (2012) The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Applied Microbiology and Biotechnology 96, 1455–1464.
The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind.Crossref | GoogleScholarGoogle Scholar |

Garcia del Moral L, Rharrabti Y, Villegas D, Royo C (2003) Evaluation of grain yield and its components in durum wheat under Mediterranean conditions. Agronomy Journal 95, 266–274.
Evaluation of grain yield and its components in durum wheat under Mediterranean conditions.Crossref | GoogleScholarGoogle Scholar |

Ghabooli M, Khatabi B, Ahmadi FS, Sepehri M, Mirzaei M, Amirkhani A, Jorrín-Novo JV, Salekdeh GH (2013) Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. Journal of Proteomics 94, 289–301.
Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley.Crossref | GoogleScholarGoogle Scholar |

Gill SS, Gill R, Privedi DK, Anjum NA, Sharma KK, Ansari MW, Ansari AA, Johri AK, Prasad R, Pereira E, Varma A, Tuteja N (2016) Piriformospora indica: potential and significance in plant stress tolerance. Frontiers in Microbiology 7, 332
Piriformospora indica: potential and significance in plant stress tolerance.Crossref | GoogleScholarGoogle Scholar |

Golombek S, Al-Ramamneh ED (2002) Drought tolerance mechanisms of pearl millet. In ‘Conference on Agricultural and Natural Resource Management’. 9–11 October, University of Kassel, Institute of Crop Science, Germany.

Gong M, You X, Zhang Q (2015) Effects of Glomus intraradices on the growth and reactive oxygen metabolism of foxtail millet under drought. Annals of Microbiology 65, 595–602.
Effects of Glomus intraradices on the growth and reactive oxygen metabolism of foxtail millet under drought.Crossref | GoogleScholarGoogle Scholar |

Gosal S, Karlupia A, Gosal S, Chhibba I, Varma A (2010) Biofertilization with Piriformospora indica and Pseudomonas fluorescens improves survival rate, nutrient acquisition, field performance and saponin content of micropropagated Chlorophytum sp. Indian Journal of Biotechnology 9, 289–297.

Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology 59, 19–42.
Signaling in the arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar |

Jackson ML (1973) ‘Soil chemical analysis.’ (Prentice Hall (India): New Delhi)

Jogawat A, Saha S, Bakshi M, Dayaman V, Kumar M, Dua M, Varma A, Oelmüller R, Tuteja N, Johri AK (2013) Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signaling & Behavior 8, e26891
Piriformospora indica rescues growth diminution of rice seedlings during high salt stress.Crossref | GoogleScholarGoogle Scholar |

Kapulnik Y, Kigel J, Okon Y, Nur I, Henis Y (1981) Effect of Azospirillum inoculation on some growth parameters and N-content of wheat, sorghum and panicum. Plant and Soil 61, 65–70.
Effect of Azospirillum inoculation on some growth parameters and N-content of wheat, sorghum and panicum.Crossref | GoogleScholarGoogle Scholar |

Kramer PJ, Boyer JS (1995) ‘Water relations of plants and soils.’ (Academic Press: Cambridge, MA, USA)

Krishnaveni N, Geetha Ramani Ranjitha L, Cibichakravarthy B (2015) Novel cultivable mycobiont Piriformospora indica as plant growth promoting endophyte. Research Journal of Biological Sciences 4, 11–15.

Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155, 780–790.
Antioxidant enzyme activities in maize plants colonized with Piriformospora indica.Crossref | GoogleScholarGoogle Scholar |

Lum MR, Hirsch AM (2002) Roots and their symbiotic microbes: strategies to obtain nitrogen and phosphorus in a nutrient-limiting environment. Journal of Plant Growth Regulation 21, 368–382.
Roots and their symbiotic microbes: strategies to obtain nitrogen and phosphorus in a nutrient-limiting environment.Crossref | GoogleScholarGoogle Scholar |

Mahalakshmi V, Bidinger FR (1985) Water stress and time of floral initiation in pearl millet. Journal of Agricultural Science 105, 437–445.

Malla R, Varma A (2004) Phosphatase(s) from microorganisms. In ‘Biotechnological applications of microbes’. (Eds A Varma, GK Podila) pp. 125–150. (I.K. International: New Delhi)

Molz FJ, Klepper B (1973) On the mechanism of water-stress-induced stem deformation. Agronomy Journal 65, 304–306.
On the mechanism of water-stress-induced stem deformation.Crossref | GoogleScholarGoogle Scholar |

Nagarajan S, Nagarajan S (2010) Abiotic tolerance and crop improvement. In ‘Abiotic stress adaptation in plants: physiological, molecular and genomic foundation’. (Eds A Pareek, SK Sopory, H Bohnert, Govindjee) pp. 1–11. (Springer: Dordrecht, The Netherlands)

Nagaz K, Masmoudi M, Mechila N (2009) Yield and water use-efficiency of pearl millet (Pennisetum glaucum (L.) R. Br.) under deficit irrigation with saline water in arid conditions of Southern Tunisia. Research Journal of Agronomy 3, 9–17.

Nautiyal CS, Chauhan PS, DasGupta SM, Seem K, Varma A, Staddon WJ (2010) Tripartite interactions among Paenibacillus lentimorbus NRRL B-30488, Piriformospora indica DSM 11827, and Cicer arietinum L. World Journal of Microbiology & Biotechnology 26, 1393–1399.
Tripartite interactions among Paenibacillus lentimorbus NRRL B-30488, Piriformospora indica DSM 11827, and Cicer arietinum L.Crossref | GoogleScholarGoogle Scholar |

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

Omirou M, Ioannides IM, Ehaliotis C (2013) Mycorrhizal inoculation affects arbuscular mycorrhizal diversity in watermelon roots, but leads to improved colonization and plant response under water stress only. Applied Soil Ecology 63, 112–119.
Mycorrhizal inoculation affects arbuscular mycorrhizal diversity in watermelon roots, but leads to improved colonization and plant response under water stress only.Crossref | GoogleScholarGoogle Scholar |

Pham GH, Kumari R, Singh A, Malla R, Prasad R, Sachdev M, Kaldorf M, Buscot F, Oelmüller R, Hampp R (2008) Axenic culture of symbiotic fungus Piriformospora indica. In ‘Plant surface microbiology’. (Eds A Varma, L Abbott, D Werner, R Hampp) pp. 593–613. (Springer: Berlin, Heidelberg)

Pinkerton A, Simpson J (1986) Interactions of surface drying and subsurface nutrients affecting plant growth on acidic soil profiles from an old pasture. Animal Production Science 26, 681–689.
Interactions of surface drying and subsurface nutrients affecting plant growth on acidic soil profiles from an old pasture.Crossref | GoogleScholarGoogle Scholar |

Puangbut D, Jogloy S, Vorasoot N, Akkasaeng C, Kesmalac T, Patanothai A (2009) Variability in yield responses of peanut (Arachis hypogaea L.) genotypes under early season drought. Asian Journal of Plant Sciences 8, 254–264.
Variability in yield responses of peanut (Arachis hypogaea L.) genotypes under early season drought.Crossref | GoogleScholarGoogle Scholar |

Rai M, Varma A (2005) Arbuscular mycorrhiza-like biotechnological potential of Piriformospora indica, which promotes the growth of Adhatoda vasica Nees. Electronic Journal of Biotechnology 8, 1–6.
Arbuscular mycorrhiza-like biotechnological potential of Piriformospora indica, which promotes the growth of Adhatoda vasica Nees.Crossref | GoogleScholarGoogle Scholar |

Rai M, Acharya D, Singh A, Varma A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11, 123–128.
Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial.Crossref | GoogleScholarGoogle Scholar |

Rao S, Qayyum A, Razzaq A, Ahmad M, Mahmood I, Sher A (2012) Role of foliar application of salicylic acid and L-tryptophan in drought tolerance of maize. Journal of Animal and Plant Sciences 22, 768–772.

Rathod D, Brestic M, Shao H (2011) Chlorophyll a fluorescence determines the drought resistance capabilities in two varieties of mycorrhized and non-mycorrhized Glycine max Linn. African Journal of Microbiological Research 24, 4197–4206.

Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. Journal of Experimental Botany 59, 1109–1114.
More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis.Crossref | GoogleScholarGoogle Scholar |

Sasani S, Jahansooz MR, Ahmadi A (2004) The effects of deficit irrigation on water use efficiency, yield and quality of forage pearl millet. In ‘Proceedings 4th International Crop Science Congress’. 26 Sept.–1 Oct., Brisbane, Qld. (The Regional Institute: Gosford, NSW)

Seghatoleslami M, Kafi M, Majidi E (2008) Effect of drought stress at different growth stages on yield and water use efficiency of five proso millet (Panicum miliaceum L.) genotypes. Pakistan Journal of Botany 40, 1427–1432.

Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller R (2005) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. The Journal of Biological Chemistry 280, 26241–26247.
The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters.Crossref | GoogleScholarGoogle Scholar |

Sherameti I, Tripathi S, Varma A, Oelmüller R (2008) The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Molecular Plant-Microbe Interactions 21, 799–807.
The root-colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves.Crossref | GoogleScholarGoogle Scholar |

Singh A, Sharma J, Rexer KH, Varma A (2000) Plant productivity determinants beyond minerals, water and light: Piriformospora indica, a revolutionary plant growth promoting fungus. Current Science 79, 1548–1554.

Singh A, Singh A, Kumari M, Rai MK, Varma A (2003) Biotechnological importance of Piriformospora indica Verma et al—a novel symbiotic mycorrhiza-like fungus: an overview. Indian Journal of Biotechnology 2, 65–75.

Singh S, Gupta A, Kaur N (2012) Differential responses of antioxidative defence system to long‐term field drought in wheat (Triticum aestivum L.) genotypes differing in drought tolerance. Journal of Agronomy & Crop Science 198, 185–195.
Differential responses of antioxidative defence system to long‐term field drought in wheat (Triticum aestivum L.) genotypes differing in drought tolerance.Crossref | GoogleScholarGoogle Scholar |

Smirnoff N (1995) Antioxidant systems and plant response to the environment. In ‘Environment and plant metabolism. Environmental plant biology series’. (Ed. N Smirnoff) pp. 217–243. (Bios Scientific Publishers: Oxford, UK)

Subramanian KS, Charest C (1998) Arbuscular mycorrhiza and nitrogen assimilation in maize after drought and recovery. Physiologia Plantarum 102, 285–296.
Arbuscular mycorrhiza and nitrogen assimilation in maize after drought and recovery.Crossref | GoogleScholarGoogle Scholar |

Subramanian K, Charest C, Dwyer L, Hamilton R (1995) Arbuscular mycorrhizas and water relations in maize under drought stress at tasselling. New Phytologist 129, 643–650.
Arbuscular mycorrhizas and water relations in maize under drought stress at tasselling.Crossref | GoogleScholarGoogle Scholar |

Sun C, Johnson JM, Cai D, Sherameti I, Oelmüller R, Lou B (2010) 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. Journal of Plant Physiology 167, 1009–1017.
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.Crossref | GoogleScholarGoogle Scholar |

van Oosterom E, Bidinger F, Weltzien E (2003) A yield architecture framework to explain adaptation of pearl millet to environmental stress. Field Crops Research 80, 33–56.
A yield architecture framework to explain adaptation of pearl millet to environmental stress.Crossref | GoogleScholarGoogle Scholar |

Varma A, Verma S, Sahay N, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Applied and Environmental Microbiology 65, 2741–2744.

Varma A, Singh A, Sahay NS, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D, Bharti K (2001) Piriformospora indica: an axenically culturable mycorrhiza-like endosymbiotic fungus. In ‘Fungal associations’. (Ed. B Hock) pp. 125–150. (Springer: Berlin, Heidelberg)

Varma A, Bakshi M, Lou B, Hartmann A, Oelmueller R (2012) Piriformospora indica: a novel plant growth-promoting mycorrhizal fungus. Agricultural Research 1, 117–131.
Piriformospora indica: a novel plant growth-promoting mycorrhizal fungus.Crossref | GoogleScholarGoogle Scholar |

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

Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences of the United States of America 102, 13386–13391.
The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield.Crossref | GoogleScholarGoogle Scholar |

Winkel T, Payne W, Renno JF (2001) Ontogeny modifies the effects of water stress on stomatal control, leaf area duration and biomass partitioning of Pennisetum glaucum. New Phytologist 149, 71–82.
Ontogeny modifies the effects of water stress on stomatal control, leaf area duration and biomass partitioning of Pennisetum glaucum.Crossref | GoogleScholarGoogle Scholar |

Zegada-Lizarazu W, Iijima M (2005) Deep root water uptake ability and water use efficiency of pearl millet in comparison to other millet species. Plant Production Science 8, 454–460.
Deep root water uptake ability and water use efficiency of pearl millet in comparison to other millet species.Crossref | GoogleScholarGoogle Scholar |