Skip to main content
SpringerLink
Log in

Effects of Piriformospora indica on the growth, fruit quality and interaction with Tomato yellow leaf curl virus in tomato cultivars susceptible and resistant to TYCLV

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Tomato yellow leaf curl virus (TYLCV) resistant cultivar T07-4 and susceptible cultivar T07-1 were inoculated with the root endophytic fungus, Piriformospora indica in greenhouse to study the effects of P. indica inoculation on the tomato growth, early yield, fruit quality and resistance to TYCLV. The results indicated that P. indica stimulated root growth, promoted the growth of tomato plants between 2–6 weeks for T07-1 and 2–4 weeks for T07-4 cultivar after inoculation. The early fruit yield was improved by 12.8 % for susceptible cultivar T07-1, but no significant difference for resistant cultivar T07-4. The taste of fruits are even better because of higher ratio of TSS to TA for two cultivars and P. indica increased TSS and firmness for cultivar T07-1. P. indica enhanced more pathogensis-related genes expressions in inoculated susceptible cultivar T07-1 than in resistant cultivar T07-4 at 2 weeks after inoculation. P. indica induced resistance against TYCLV for susceptible cultivar, reduced TYCLV incidence and decreased disease index by 26 % and 1.25 in natural TYCLV infection. One may draw an inference that P. indica inoculation can lead to better vegetative growth, higher early yield and induced resistance for TYLCV-susceptiable cultivar T07-1 in practical greenhouse condition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

P. indica :

Piriformospora indica

AMF:

Arbuscular mycorrhizal fungi

TYLCV:

Tomato yellow leaf curl virus

EC:

Electrical conductivity

DW:

Dry weight

TSS:

Total soluble solid

TA:

Titratable acidity

AA:

Ascorbic acid

RNA:

Ribonucleic acid

RT-PCR:

Reverse transcription-polymerase chain reaction

PR:

Pathogenesis-related

SAR:

Systemic acquired resistance

SA:

Salicylic acid

ISR:

Induced systemic resistance

References

  • Andrade-Linares DR, Muller A, Fakhro A, Schwarz A, Frankan P (2013) Piriformospora indica, Sebacinales and their biotechnological applications. Soil Biol 33:107–117

    Google Scholar 

  • Deshmukh SD, Kogel KH (2007) Piriformospora indica protects barley from root rot caused by Fusarium graminearum. J Plant Dis Prot 114:263–268

    Google Scholar 

  • Deshmukh S, Hueckelhoven R, Schafer P, Imani J, Sharma M, Weiss M, Waller F, Kogel KH (2006) The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc Natl Acad Sci USA 103:18450–18457

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dolatabadi HK, Goltapeh EM, Jaimand K, Rohani N, Varma A (2011) Effects of Piriformospora indica and Sebacina vermifera on growth and yield of essential oil in fennel (Foeniculum vulgare) under greenhouse conditions. J Basic Microbiol 51:33–39

    Article  CAS  PubMed  Google Scholar 

  • Dorais M, Ehret DL, Papadopoulos AP (2008) Tomato (Solanum lycopersicum) health components: from the seed to the consumer. Phytochem Rev 7:231250. doi:10.1007/s11101-007-9085-x

    Google Scholar 

  • Fakhro A, Andrade-Linares DR, von Bargen S, Bandte M, Buttner C, Grosch R, Schwarz D, Franken P (2010) Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20:191–200

    Article  PubMed  Google Scholar 

  • Franken P (2012) The plant strengthening root endophyte Piriformospora indica: potential application and the biology behind. Appl Microbiol Biotechnol 96:1455–1464

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Franzini VI, Azcon R, Mendes FL, Aroca R (2013) Different interaction among Glomus and Rhizobium species on Phaseolus vulgaris and Zea mays plant growth, physiology and symbiotic development under moderate drought stress conditions. Plant Growth Regul 70:265–273. doi:10.1007/s10725-013-9798-3

    Article  CAS  Google Scholar 

  • Friedmann M, Lapidot M, Cohen S, Pilowsky M (1998) A novel source of resistance to tomato yellow leaf curl virus exhibiting a symptomless reaction to viral infection. J Am Soc Hortic Sci 123:1004–1007

    Google Scholar 

  • Frohlich DR, Torres-Jerez I, Bedford ID, Markham PG, Brown JK (2002) A phylogeographical analysis of the Bemisia tabaci species complex based on mito-chondrial DNA markers. Mol Ecol 8:1683–1691

    Article  Google Scholar 

  • Ghanim M, Morin S, Czosnek H (2001) Rate of Tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 91:188–196. doi:10.1094/phyto.2001.91.2.188

    Article  CAS  PubMed  Google Scholar 

  • Glick E, Levy Y, Gafni Y (2009) The viral etiology of Tomato yellow leaf curl disease—a review. Plant Prot Sci 45:81–97

    CAS  Google Scholar 

  • Guil-Guerrero JL, Rebolloso-Fuentes MM (2009) Nutrient composition and antioxidant activity of eight tomato (Lycopersicon esculentum) varieties. J Food Compos Anal 22:123–129

    Article  CAS  Google Scholar 

  • Hanssen IM, Lapidot M, Thomma BP (2010) Emerging viral diseases of Tomato crops. Mol Plant Microbe Interact 23:539–548

    Article  CAS  PubMed  Google Scholar 

  • Heber D (2000) Colorful cancer prevention: alpha-carotene, lycopene, and lung cancer. Am J Clin Nutr 72:901–902

    CAS  PubMed  Google Scholar 

  • Jiang F, Zheng XD, Chen JS (2009) Microarray analysis of gene expression profile induced by the biocontrol yeast Cryptococcus laurentii in cherry tomato fruit. Gene 430:12–16

    Article  PubMed  Google Scholar 

  • Khatabi B, Molitor A, Lindermayr C, Pfiffi Durner S, Wettstein DV, Kogel KH, Schafer P (2012) Ethylene supports colonization of plant roots by the mutualistic fungus Piriformospora indica. PLos One. 035502. http://www.plosone.org/article/info:doi/10.1371/journal.pone

  • Kumar Praveen G, Kishore N, Amalraj Daniel EL, Ahmed Hassan SKM, Rasul A, Desai S (2012) Evaluation of fluorescent Pseudomonas spp. with single and multiple PGPR traits for plant growth promotion of sorghum in combination with AM fungi. Plant Growth Regul 67:133–140. doi:10.1007/s10725-012-9670-x

    Article  Google Scholar 

  • Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544

    Article  CAS  PubMed  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Mugiira RB, Liu SS, Zhou XP (2008) Tomato yellow leaf curl virus and Tomato leaf curl Taiwan virus invade south-east coast of China. J Phytopathology 156:217–221

    Article  CAS  Google Scholar 

  • Oelmuller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17

    Article  Google Scholar 

  • Peškan-Berghöfer T, Shahollari B, Giang PH, Hehl S, Markert C, Blanke V, Varma AK, Oelmüller R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmatic reticulum and at the plasma membrane. Physiol Plant 122:465–477

    Article  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  PubMed  Google Scholar 

  • Sarma MVRK, Kumar V, Saharan K, Srivastava R, Sharma AK, Prakash A, Sahai V, Bisaria VS (2011) Application of inorganic carrier-based formulations of fluorescent pseudomonads and Piriformospora indica on tomato plants and evaluation of their efficacy. J Appl Microbiol 111:456–466

    Article  CAS  PubMed  Google Scholar 

  • Schafer P, Pfiffi S, Voll L, Zajic D, Chandler P, Waller F, Scholz U, Pons-Kuhnemann J, Sonnewald S, Sonnewald U, Kogel KH (2009) Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 59:461–474

    Article  PubMed  Google Scholar 

  • Serfling A, Wirsel SGR, Lind V, Deising HB (2007) Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathology 97:523–531

    Article  CAS  PubMed  Google Scholar 

  • Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmuller 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 which binds to a conserved motif in their promoters. J Biol Chem 280:2641–2647

    Article  Google Scholar 

  • Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM, Nitz I, Varma A, Grundler FM, Oelmuller R (2008) PYK10, a beta-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 54:428–439

    Article  CAS  PubMed  Google Scholar 

  • Shoresh M, Harman GE (2008) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147:2147–2163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shoresh M, Yedidia I, Chet I (2005) Involvement of jasmonic acid/ethylene signalling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95:76–84

    Article  CAS  PubMed  Google 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. Curr Sci 79:1548–1554

    Google Scholar 

  • Sirrenberg A, Goebel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K (2007) Piriformospora indica affects plant growth by auxin production. Physiol Plant 131:581–589

    Article  CAS  PubMed  Google Scholar 

  • Smith S, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, London

  • Stein E, Molitor A, Kogel K-H, 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

    Article  CAS  PubMed  Google Scholar 

  • Sun C, Johnson J, Cai DG, Sherameti I, Oelmuller R, Lou BG (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

    Article  CAS  PubMed  Google Scholar 

  • Tian AM, Cao JS, Huang L, Yu XL, Ye WZ (2009) Characterization of a male sterile related gene BcMF15 from Brassica campestris ssp. chinensis. Mol Biol Rep 36:307–314

    Article  CAS  PubMed  Google Scholar 

  • Toor RK, Savage GP (2005) Antioxidant activity in different fractions of tomatoes. Food Res Int 38:487–494

    Article  CAS  Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathology 36:453–458

    Article  Google Scholar 

  • Van Peer R, Niemann GJ, Schnippers B (1991) Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 91:728–734

    Article  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11:443–448

    Article  PubMed  Google Scholar 

  • Varma A, Verma S, Sudah SN, Franken P (1999) Piriformospora indica, a cultivable plant growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744

    CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Waller F, Mukherjee K, Deshmukh SD, Achatz B, Sharma M, Schäfer P, Kogel KH (2008) Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. J Plant Physiol 165:60–70

    Article  CAS  PubMed  Google Scholar 

  • Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander D, Ahl-Goy P, Metraux JP, Ryals JA (1991) Coordinate gene activity in response to agents those induce systemic acquired resistance. Plant Cell 3:1085–1094

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wei G, Kloepper JW, Tuzun S (1991) Induction of systemic resistance of cucumber to Colletotrichum orbiculare by selected strains of plant-growth promoting rhizobacteria. Phytopathology 81:1508–1512

    Article  Google Scholar 

  • Wright KP, Kader AA (1997) Effect of controlled-atmosphere storage on the quality and carotenoid content of sliced persimmons and peaches. Postharvest Biol Technol 10:89–97

    Article  Google Scholar 

  • Wu JB, Dai FM, Zhou XP (2006) First report of Tomato yellow leaf curl virus in China. Ann Appl Biol 155:439–448

    Google Scholar 

  • 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. doi:10.1007/s10725-012-9690-6

    Article  CAS  Google Scholar 

  • Yang B, Wang XM, Ma HY, Jia Y, Li X, Dai CC (2014) Effects of the fungal endophyte Phomopsis liquidambari on nitrogen uptake and metabolism in rice. Plant Growth Regul 73:165–179

    Article  CAS  Google Scholar 

  • Yooyongwech S, Phaukinsang N, Chaum S, Supaibulwatana K (2013) Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regul 69:285–293

    Article  CAS  Google Scholar 

  • Zheng JR, Wang HL, Wang JM (2010) A new tomato F1 hybrid with resistance to TYLCV—‘Hangza No. 301’. China Veg 8:80–82

    Google Scholar 

  • 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 KH (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7:e1002290

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by grants from National Key Technology R&D Program of China (2012BAD33B08), the Ph.D. Programs Foundation of Ministry of Education of China (20100101110087), National Natural Science Foundation of China (30972051, 31460411, 31260402 and 21362028), Special Fund for Agro-scientific Research in the Public Interest (20090304), Program for Key Innovative Research Team of Zhejiang Province and Safety Controlling and Intensive Processing of Distinctive Agricultural Products of Hangzhou City.

Author information

Author notes

    Authors and Affiliations

    1. School of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou, 310058, Zhejiang, China

      Huili Wang, Ting Yu & Xiaodong Zheng

    2. Hangzhou Wanxiang Polytechnic, Hangzhou, 310023, Zhejiang, China

      Huili Wang

    3. Department of Vegetable, Hangzhou Academy of Agricultural Sciences, Hangzhou, 310024, China

      Jirong Zheng

    4. College of Food Engineering and Nutritional Science, Shanxi Normal University, Xi’an, 710119, Shanxi, China

      Xueyan Ren

    5. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, India

      Ajit Varma

    6. Institute of Biotechnology, Zhejiang University, Hangzhou, 310058, Zhejiang, China

      Binggan Lou

    Authors
    1. Huili Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Jirong Zheng
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Xueyan Ren
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Ting Yu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Ajit Varma
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Binggan Lou
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Xiaodong Zheng
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Xiaodong Zheng.

    Additional information

    Huili Wang and Jirong Zheng have contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 16 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Wang, H., Zheng, J., Ren, X. et al. Effects of Piriformospora indica on the growth, fruit quality and interaction with Tomato yellow leaf curl virus in tomato cultivars susceptible and resistant to TYCLV. Plant Growth Regul 76, 303–313 (2015). https://doi.org/10.1007/s10725-015-0025-2

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10725-015-0025-2

    Keywords

    Search

    Navigation