Abstract
Serendipita indica (formerly known as Piriformospora indica), a root endophytic fungus, exhibits multiple functions in some agricultural, horticultural, and medicinal plant species. We studied colonization of the roots of Platycladus orientalis, a forest tree species, by S. indica to improve the quality of the seedlings in seedbeds and survival rates in sylviculture. At 20 days after inoculation, S. indica colonized the root cortex of P. orientalis seedlings. Root colonization by S. indica significantly increased net CO2 assimilation, light use efficiency, and biomass accumulation by both roots and shoots, whereas it did not affect the biomass allocation between roots and shoots. In addition, the symbiosis significantly increased root total length, surface area, and volume. In view of the two specific traits of S. indica, i.e., axenic culture and wide colonization in plants, the fungus might be used for improving quality of P. orientalis seedlings and increasing their survival after transplanting.
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Achatz B, Kogel KH, Franken P, Waller F (2010) Piriformospora indica mycorrhization increases grain yield by accelerating early development of barley plants. Plant Signal Beha 5:1685–1687
Arora M, Saxena P, Choudhary DK, Abdin MZ, Varma A (2016) Dual symbiosis between Piriformospora indica and Azotobacter chroococcum enhances the artemisinin content in Artemisia annua L. World J Microbiol Biotechnol 32(2):19. https://doi.org/10.1007/s11274-015-1972-5
Badde US, Prasad R, Varma A (2015) Interaction of mycobiont: Piriformospora indica with medicinal plants and plants of economic importance. Afr J Biotechnol 9(54):9214–9226
Bakshi M, Sherameti I, Johri AK, Varma A, Oelmüller R (2014) Phosphate availability affects root architecture and development, plant performance and is controlled by root-colonizing microbes. J Endocytobiosis Cell Res 25:56–65
Bakshi M, Vahabi K, Bhattacharya S, Sherameti I, Varma A, Yeh K-W, Baldwin I, Johri AK, Oelmüller R (2015) WRKY6 restricts Piriformospora indica-stimulated and phosphate-induced root development in Arabidopsis. BMC Plant Biol 15:305. https://doi.org/10.1186/s12870-015-0673-4
Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–510
Bán R, Baglyas G, Virányi F, Barna B, Posta K, Kiss J, Körösi K (2017) The chemical inducer, BTH (benzothiadiazole) and root colonization by mycorrhizal fungi (Glomus spp.) trigger resistance against white rot (Sclerotinia sclerotiorum) in sunflower. Acta Biol Hung 68(1):50–59
Berta G, Trotta A, Fusconi A, Hooker JE, Munro M, Atkinson D, Giovannetti M, Morini S, Fortuna P, Tisserant B, Gianinazzi-Pearson V, Gianinazzi S (1995) Arbuscular mycorrhizal induced changes to plant growth and root system morphology in Prunus cerasifera. Tree Physiol 15:281–294
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185
Brown AC, Sinclair WA (1981) Colonization and infection of primary roots of Douglas-fir seedlings by the ectomycorrhizal fungus Laccaria laccata. For Sci 27:111–124
Bruisson S, Maillot P, Schellenbaum P, Walter B, Gindro K, Deglene-Benbrahim L (2016) Arbuscular mycorrhizal symbiosis stimulates key genes of the phenylpropanoid biosynthesis and stilbenoid production in grapevine leaves in response to downy mildew and grey mould infection. Phytochemistry 131:92–99
Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmüller R (2011) The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog 7(5):e1002051. https://doi.org/10.1371/journal.ppat.1002051
Cordell CE, Owen HI, Marx DH (1987) Mycorrhizae nursery management for improved seedling quality and field performance. In: Proceedings of intermountain for nursery association, Aug 10–14, 1987, pp 105–115
Daneshkhah R, Cabello S, Rozanska E, Sobczak M, Grundler FMW, Wieczorek K, Hofmann J (2013) Piriformospora indica antagonizes cyst nematode infection and development in Arabidopsis roots. J Exp Bot 64:3763–3774
Das A, Tripathi S, Varma A (2014) In vitro plant development and root colonization of Coleus forskohlii by Piriformospora indica. World J Microbiol Biotechnol 30:1075–1084
Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128:79–87
García IV, Mendoza RE (2007) Arbuscular mycorrhizal fungi and plant symbiosis in a saline-sodic soil. Mycorrhiza 17:167–174
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Glen M, Tommerup IC, Bougher NL, O’Brien PA (2002) Are Sebacinaceae common and widespread ectomycorrhizal associates of Eucalyptus species in Australian forests? Mycorrhiza 12:243–247
Habte M, Miyasaka SC, Matsuyama DT (2001) Arbuscular mycorrhizal fungi improve early forest-tree establishment. In: Horst WJ, Schenk MK, Bürkert A, Claassen N, Flessa H, Frommer WB, Goldbach H, Olfs H-W, Römheld V, Sattelmacher B, Schmidhalter U, Schubert S, von Wirén N, Wittenmayer L (eds) Plant nutrition: food security and sustainability of agroecosystems. Kluwer Academic Publishers, Dordrecht, pp 644–645
Harrach BD, Baltruschat H, Barna B, Fodor J, Kogel K-H (2013) The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Mol Plant Microbe Int 26:599–605
Hooker JE, Munro M, Atkinson D (1992) Vesicular–arbuscular mycorrhizal fungi induced alteration in poplar root system morphology. Plant Soil 145:207–214
Hosseini F, Mosaddeghi MR, Dexter AR (2017) Effect of the fungus Piriformospora indica on physiological characteristics and root morphology of wheat under combined drought and mechanical stresses. Plant Physiol Biochem 118:107–120
Javaid A (2009) Arbuscular mycorrhizal mediated nutrition in plants. J Plant Nutr 32:1595–1618
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 Signal Behav 8:e26891. https://doi.org/10.4161/psb.26891
Johnson JM, Sherameti I, Ludwig A, Nongbri PL, Sun C, Lou B, Varma A, Oelmuller R (2011) Protocols for Arabidopsis thaliana and Piriformospora indica co-cultivation—a model system to study plant beneficial traits. J Endocytobiosis Cell Res 21:101–113
Khalvati M, Bartha B, Dupigny A, Schröder P (2010) Arbuscular mycorrhizal association is beneficial for growth and detoxification of xenobiotics of barley under drought stress. J Soils Sediments 10:54–64
Kharkwal AC, Prasad R, Kharkwal H, Das A, Bhatnagar K, Sherameti I, Oelmüller R, Varma A (2007) Co-cultivation with sebacinales. In: Varma A, Oelmüller R (eds) Advanced techniques in soil microbiology. Springer, Berlin, pp 247–270
Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New flux parameters for the determination of QA redox state and excitation fluxes. Photosynthesis Res 79:209–218
Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790
Kumar M, Yadav V, Kumar H, Sharma R, Singh A, Tuteja N, Johri AK (2011) Piriformospora indica enhances plant growth by transferring phosphate. Plant Signal Behav 6:723–725
Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B, Oelmüller R, Yeh KW (2011) Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol Plant Microbe Interact 24:421–431
Li Y, Zhang W, Shen J, Zhou J, Guo Y (2015) Carbon density and its allocation characteristics of young plantation of Platycladus orientalis in the hilly Loess region of Gansu province, China. Sci Silvae Sin 51(6):1–8 (in Chinese with English abstract)
Liang M, Liu X, Etienne RS, Huang F, Wang Y, Yu S (2015) Arbuscular mycorrhizal fungi counteract the Janzen–Connell effect of soil pathogens. Ecology 96:562–574
Liu FC, Xing SJ, Ma HL, Du ZY, Ma BY (2014) Effects of drought stress on growth, nutrition and physiological characteristics of Platycladus orientalis container and bareroot seedlings. J Beijing For Univ 36(5):68–73 (in Chinese with English abstract)
Meng L, Zhang A, Wang F, Han X, Wang D, Li S (2015) Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00339
Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569
Molitor A, Kogel KH (2009) Induced resistance triggered by Piriformospora indica. Plant Signal Behav 4(3):215–216
Nongbri PL, Oelmüller R (2013) Role of Piriformospora indica in sulfur metabolism in Arabidopsis thaliana. In: Varma A, Kost G, Oelmüller R (eds) Piriformospora indica: sebacinales and their biotechnological applications. Springer, Berlin, pp 295–309
Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17
Prasad R, Kamal S, Sharma PK, Oelmuller R, Varma A (2013) Root endophyte Piriformospora indica DSM 11827 alters plant morphology, enhances biomass and antioxidant activity of medicinal plant Bacopa monniera. J Basic Microbiol 53:1016–1024
Rathod DP, Brestic M, Shao HB (2011) Chlorophyll a fluorescence determines the drought resistance capabilities in two varieties of mycorrhized and non-mycorrhized Glycine max Linn. Afr J Microbiol Res 5:4197–4206
Reidinger S, Eschen R, Gange AC, Finch P, Bezemer TM (2012) Arbuscular mycorrizal colonization, plant chemistry, and aboveground herbivory on Senecio jacobaea. Acta Oecol 38:8–16
Schellenbaum L, Berta G, Ravolanirina F, Tisserant B, Gianinazzi S, Fitter AH (1991) Influence of endo-mycorrhizal infection on root morphology in a micro-propagated woody plant species (Vitis vinifera L.). Ann Bot 68:135–141
Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62
Sharma G, Agrawal V (2013) Marked enhancement in the artemisinin content and biomass productivity in Artemisia annua L. shoots co-cultivated with Piriformospora indica. World J Microbiol Biotechnol 29:1133–1138
Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296
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. Mol Plant Microbe Interact 21:799–807
Sinclair WA, Cowles DP, Hee SM (1975) Fusarium root rot of Douglas-fir seedlings: suppression by soil fumigation, fertility management, and inoculation with spores of the fungal symbiont Laccaria laccata. For Sci 21:390–399
Singh A, Sharma J, Rexer K-H, Varma A (2000) Plant productivity determinants beyond minerals, water and light: Piriformospora indica—a revolutionary plant growth promoting fungus. Curr Sci 79:1548–1554
Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786. https://doi.org/10.3389/fpls.2015.00786
Stein E, Molitor A, Kogel KH, Waller F (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 49:1747–1751
Strobel NE, Sinclair WA (1991a) Influence of temperature and pathogen aggressiveness on biological control by Laccaria bicolor of Fusarium root rot of Douglas-fir. Phytopathology 81:415–420
Strobel NE, Sinclair WA (1991b) Role of flavanolic wall infusions in the resistance induced by Laecaria bieolor to Fusarium oxysporum in primary roots of Douglas-fir. Phytopathology 81:420–425
Strobel NE, Sinclair WA (1992) Role of mycorrhizal fungi in tree defense against fungal pathogens of roots. In: Blanchette RA, Biggs AR (eds) Defense mechanisms of woody plants against fungi. Springer, Berlin, pp 321–352
Su ZZ, Wang T, Shrivastava N, Chen YY, Liu X, Sun C, Yin Y, Gao QK, Lou BG (2017) Piriformospora indica promotes growth, seed yield and quality of Brassica napus L. Microbiol Res 199:29–39
Sun C, Johnson J, Cai D, Sherameti I, Oelmüeller 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. J Plant Physiol 167:1009–1017
Sun C, Shao Y, Vahabi K, Lu J, Bhattacharya S, Dong S, Ye K-W, Sherameti I, Lou B, Baldwin I, Oelmüller R (2014) The beneficial fungus Piriformospora indica protects Arabidopsis from Verticillium dahliae infection by downregulation plant defense responses. BMC Plant Biol 14:268. https://doi.org/10.1186/s12870-014-0268-5
Tabrizi L, Mohammadi S, Delshad M, Moteshare Zadeh B (2015) Effect of arbuscular mycorrhizal fungi on yield and phytoremediation performance of pot marigold (Calendula officinalis L.) under heavy metals stress. Int J Phytoremediation 17:1244–1252
Tao L, Ahmad A, de Roode JC, Hunter MD (2016) Arbuscular mycorrhizal fungi affect plant tolerance and chemical defences to herbivory through different mechanisms. J Ecol 104:561–571
Tisserant B, Schellenbaum L, Gianinazzi-Pearson V, Gianinazzi S, Berta G (1992) Influence of infection by an endomycorrhizal fungus on root development and root architecture in Platanus acerifolia. Allionia 30:171–181
Unnikumar KR, Sree SK, Varma A (2013) Piriformospora indica: a versatile root endophytic symbiont. Symbiosis 60:107–113
Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. MPMI 21:1371–1383
Vadassery J, Ranf S, Drzewiecki C, Mithofer A, Mazars C, Scheel D, Lee J, Oelmüller R (2009) A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59:193–206
Vahabi K, Johnson JM, Drzewiecki C, Oelmüller R (2011) Fungal staining tools to study the interaction between the beneficial endophyte Piriformospora indica with Arabidopsis thaliana roots. J Endocytobiosis Cell Res 21:77–88
van Kooten O, Snel J (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150
Varma A, Verma S, Suhha Sahay N, Butehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744
Varma A, Singh A, Sudha Sahay NS, Sharma J, Roy A, Kumari M, Rana D, Thakran S, Deka D, Bharti K, Hurek T, Blechert O, Rexer K-H, Kost G, Hahn A, Hock B, Maier W, Walter M, Strack D, Kranner I (2001) Piriformospora indica: an axenically culturable mycorrhiza-like endosymbiotic fungus. In: Hock B (ed) Fungal associations. Springer, New York, pp 125–150
Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–217
Verma S, Varma A, Rexer KH, Hassel A, Kost G, Sarbhoy A, Bisen P, Butehorn B, Fraken P (1998) Piriformospora indica, gen. et sp. nov., a new root colonizing fungus. Mycologia 9:896–903
Wang YM, Liu BZ (1994) Shelter-forest ecological characteristics on semi-arid region of the loess plateau. China Forestry Press, Beijing, pp 105–132 (in Chinese)
Watts-Williams SJ, Jakobsen I, Cavagnaro TR, Gronlund M (2015) Local and distal effects of arbuscular mycorrhizal colonization on direct pathway Pi uptake and root growth in Medicago truncatula. J Exp Bot 66:4061–4073
Wu QS, He XH, Zou YN, Liu CY, Xiao J, Li Y (2012) Arbuscular mycorrhizas alter root system architecture of Citrus tangerine through regulating metabolism of endogenous polyamines. Plant Growth Regul 68:27–35
Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544
Yang H, Zhang Q, Dai Y, Liu Q, Tang J, Bian X, Chen X (2015) Effects of arbuscular mycorrhizal fungi on plant growth depend on root system: a meta-analysis. Plant Soil 389:361–374
Ye W, Shen CH, Lin Y, Chen PJ, Xu X, Oelmüller R, Yeh KW, Lai Z (2014) Growth promotion-related miRNAs in Oncidium orchid roots colonized by the endophytic fungus Piriformospora indica. PLoS ONE 9:e84920. https://doi.org/10.1371/journal.pone.0084920
Zamani J, Hajabbasi M, Alaie E, Sepehri M, Leuchtmann A, Schulin R (2016) The effect of Piriformospora indica on the root development of maize (Zea mays L.) and remediation of petroleum contaminated soil. Int J Phytoremediation 18:278–287
Zarea MJ, Hajinia S, Karimi N, Mohammadi Goltapeh E, Rejali F, Varma A (2012) Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol Biochem 45:139–146
Zhang H, Franken P (2014) Comparison of systemic and local interactions between the arbuscular mycorrhizal fungus Funneliformis mosseae and the root pathogen Aphanomyces euteiches in Medicago truncatula. Mycorrhiza 24:419–430
Zou YN, Huang YM, Wu QS, He XH (2015) Mycorrhiza-induced lower oxidative burst is related with higher antioxidant enzyme activities, net H2O2 effluxes, and Ca2+ influxes in trifoliate orange roots under drought stress. Mycorrhiza 25:143–152
Zuccaro A, Lahrmann U, Guldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M, Murat C, Martin F, Kogel K-H (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7(10):e1002290. https://doi.org/10.1371/journal.ppat.1002290
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Project funding: This study was funded by National Nature Science Foundation of China (31471496).
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Corresponding editor: Zhu Hong.
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Wu, C., Wei, Q., Deng, J. et al. Changes in gas exchange, root growth, and biomass accumulation of Platycladus orientalis seedlings colonized by Serendipita indica. J. For. Res. 30, 1199–1207 (2019). https://doi.org/10.1007/s11676-018-0712-8
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DOI: https://doi.org/10.1007/s11676-018-0712-8