A Split-Root Method to Study Systemic and Heritable Traits Induced by Trichoderma in Tomato Plants
- Morán-Diez, M. E.
- Hermosa, R. 1
- de Medeiros, H. A.
- Castillo, P.
- Monte, E. 1
- Rubio, M. B. 1
- 1 Department of Microbiology and GeneticsSpanish-Portuguese Institute for Agricultural Research (CIALE), University of SalamancaSalamancaSpain
Verlag: Springer
ISSN: 2523-8442, 2523-8450
ISBN: 9789811357664, 9789811357671
Datum der Publikation: 2019
Seiten: 151-166
Art: Buch-Kapitel
Zusammenfassung
The split-root methodology constitutes an excellent tool to study local versus systemic plant-induced responses. In the most common approach, two different organisms coinfect the two separated root halves of a same plant. Split-root plants have been used to study the biocontrol potential of fungi and bacteria by the induction of systemic defenses in the plant against bacterial, fungal, oomycete, and nematode diseases and insect pests. In our particular case study, we applied this methodology to demonstrate the systemic and heritable effects induced by the biocontrol strain Trichoderma atroviride T11 in tomato plants which were tested against the root-knot nematode (RKN) Meloidogyne javanica (Mj), a major tomato pathogen worldwide. This approach allows Trichoderma and the root pathogen to be kept separate for the analysis of the T11 effects on the penetration, development, and reproduction of Mj in tomato roots upon activating plant systemic responses. The method also enables the plant green mass and nematode infection parameters to be determined and the gene expression analysis related to systemic responses and heritable traits, in terms of defense and growth, induced by T11 when plants are infected with Mj in the progeny of split-root plants.
Bibliographische Referenzen
- Abad P, Favery B, Rosso MN, Castagnone-Sereno P (2003) Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Mol Plant Pathol 4:217–224
- Abad P, Castagnone-Sereno P, Rosso MN, De Almeida Engler J, Favery B (2009) Invasion, feeding and development. In: Perry RN, Moens M, Starr JL (eds) Root-knot nematodes. CABI Publishing, Wallingford, pp 163–181
- Aberra MB, Seah S, Sivasithamparam K (1998) Suppression of the take-all fungus (Gaeumannomyces graminis var. tritici) by a sterile red fungus through induced resistance in wheat (Triticum aestivum) seedling roots. Soil Biol Biochem 30:1457–1461
- Adam M, Heuer H, Hallmann J (2014) Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS One 9:e90402
- Akram W, Anjum T, Ali B, Ahmad A (2013) Screening of native Bacillus strains to induce systemic resistance in tomato plants against Fusarium wilt in split root system and its field applications. Int J Agric Biol 15:1289–1294
- Antonopoulos DF, Tjamos SE, Antoniou PP, Rafeletos P, Tjamos EC (2008) Effect of Paenibacillus alvei, strain K165, on the germination of Verticillium dahliae microsclerotia in planta. Biol Control 46:166–170
- Anwar SA, McKenry MV (2008) Induction of resistance and susceptibility in tomato by two Meloidogyne incognita populations. J Nematol 40:276–280
- Aryal SK, Davis RF, Stevenson KL, Timper P, Ji P (2011) Induction of systemic acquired resistance by Rotylenchulus reniformis and Meloidogyne incognita in cotton following separate and concomitant inoculations. J Nematol 43:160–165
- Boukerma L, Benchabane M, Charif A, Khelifi L (2017) Activity of plant growth promoting rhizobacteria (PGPRs) in the biocontrol of tomato Fusarium wilt. Plant Prot Sci 53:78–84
- Bybd DW, Kirkpatrick T, Barker KR (1983) An improved technique for clearing and staining plant tissues for detection of nematodes. J Nematol 15:142–143
- Cabanás CGL, Sesmero R, Valverde-Corredor A, López-Escudero FJ, Mercado-Blanco J (2017) A split-root system to assess biocontrol effectiveness and defense-related genetic responses in above-ground tissues during the tripartite interaction Verticillium dahliae-olive-Pseudomonas fluorescens PICF7 in roots. Plant Soil 417:1–20
- Castellanos-Morales V, Keiser C, Cárdenas-Navarro R, Grausgruber H, Glauninger J, García-Garrido JM, Steinkellner S, Sampedro I, Hage-Ahmed K, Illana A, Ocampo JA (2011) The bioprotective effect of AM root colonization against the soil-borne fungal pathogen Gaeumannomyces graminis var. tritici in barley depends on the barley variety. Soil Biol Biochem 43:831–834
- Castellanos-Morales V, Cárdenas-Navarro R, García-Garrido JM, Illana A, Ocampo JA, Steinkellner S, Vierheilig H (2012) Bioprotection against Gaeumannomyces graminis in barley–a comparison between arbuscular mycorrhizal fungi. Plant Soil Environ 58:256–261
- Catford JG, Staehelin C, Lerat S, Piché Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 54:1481–1487
- Chen C, Belanger RR, Benhamou N, Paulitz TC (2000) Defense enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiol Mol Plant Pathol 56:13–23
- Cohen MF, Yamasaki H, Mazzola M (2005) Brassica napus seed meal soil amendment modifies microbial community structure, nitric oxide production and incidence of Rhizoctonia root rot. Soil Biol Biochem 37:1215–1227
- Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant-Microbe Interact 11:1017–1028
- Cosme M, Lu J, Erb M, Stout MJ, Franken P, Wurst S (2016) A fungal endophyte helps plants to tolerate root herbivory through changes in gibberellin and jasmonate signaling. New Phytol 211:1065–1076
- Dababat EFA, Sikora RA (2007) Induced resistance by the mutualistic endophyte, Fusarium oxysporum strain 162, toward Meloidogyne incognita on tomato. Biocontrol Sci Tech 17:969–975
- De La Peña E, Echeverría SR, Van Der Putten WH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829–840
- Dutta S, Mishra AK, Kumar BD (2008) Induction of systemic resistance against fusarial wilt in pigeon pea through interaction of plant growth promoting rhizobacteria and rhizobia. Soil Biol Biochem 40:452–461
- Eizenberg H, Plakhine D, Ziadne H, Tsechansky L, Graber ER (2017) Non-chemical control of root parasitic weeds with biochar. Front Plant Sci 8:939
- Elsen A, Gervacio D, Swennen R, De Waele D (2008) AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18:251–256
- George M, Robert F, Bohlool B (1992) Nodulation suppression by Rhizobium leguminosarum bv. phaseoli in bean split-root systems. Symbiosis 12:95–105
- Gheysen G, Mitchum MG (2011) How nematodes manipulate plant development pathways for infection. Curr Opin Plant Biol 14:415–421
- Goswami BK, Pandey RK, Rathour KS, Bhattacharya C, Singh L (2006) Integrated application of some compatible biocontrol agents along with mustard oil seed cake and furadan on Meloidogyne incognita infecting tomato plants. J Zhejiang Univ Sci B 7:873–875
- Hao Z, Fayolle L, van Tuinen D, Chatagnier O, Li X, Gianinazzi S, Gianinazzi-Pearson V (2012) Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine. J Exp Bot 63:3657–3672
- Harman GE, Obregon MA, Samuels GJ, Lorito M (2010) Changing models for commercialization and implementation of biocontrol in the developed and developing world. Plant Dis 94:928–939
- Harris AR, Ferris H (1991) Interactions between Fusarium oxysporum f. sp. tracheiphilum and Meloidogyne spp. in Vigna unguiculata. 1. Effects of different inoculum densities on Fusarium wilt. Plant Pathol 40:445–456
- Hasky-Guenther K, Hoffmann-Hergarten S, Sikora RA (1998) Resistance against the potato cyst nematode Globodera pallida systemically induced by the rhizobacteria Agrobacterium radiobacter (G12) and Bacillus sphaericus (B43). Fundam Appl Nematol 21:511–517
- He CY, Wolyn DJ (2005) Potential role for salicylic acid in induced resistance of asparagus roots to Fusarium oxysporum f. sp. asparagi. Plant Pathol 54:227–232
- He CY, Hsiang T, Wolyn DJ (2002) Induction of systemic disease resistance and pathogen defence responses in Asparagus officinalis inoculated with nonpathogenic strains of Fusarium oxysporum. Plant Pathol 51:225–230
- Henkes GJ, Jousset A, Bonkowski M, Thorpe MR, Scheu S, Lanoue A, Schurr U, Röse US (2011) Pseudomonas fluorescens CHA0 maintains carbon delivery to Fusarium graminearum-infected roots and prevents reduction in biomass of barley shoots through systemic interactions. J Exp Bot 62:4337–4344
- Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25
- Jousset A, Rochat L, Lanoue A, Bonkowski M, Keel C, Scheu S (2011) Plants respond to pathogen infection by enhancing the antifungal gene expression of root-associated bacteria. Mol Plant-Microbe Interact 24:352–358
- Kassaw TK, Frugoli JA (2012) Simple and efficient methods to generate split roots and grafted plants useful for long-distance signaling studies in Medicago truncatula and other small plants. Plant Methods 8:38
- Kaur R, Singh RS (2007) Study of induced systemic resistance in Cicer arietinum L. due to nonpathogenic Fusarium oxysporum using a modified split root technique. J Phytopathol 155:694–698
- Khan J, Ooka JJ, Miller SA, Madden LV, Hoitink HAJ (2004) Systemic resistance induced by Trichoderma hamatum 382 in cucumber against Phytophthora crown rot and leaf blight. Plant Dis 88:280–286
- Khan Z, Son SH, Akhtar J, Gautam NK, Kim YH (2012) Plant growth-promoting rhizobacterium (Paenibacillus polymyxa) induced systemic resistance in tomato (Lycopersicon esculentum) against root-knot nematode (Meloidogyne incognita). Indian J Agric Sci 82:603–607
- Khaosaad T, Garcia-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39:727–734
- LaMondia JA (2003) Interaction of Pratylenchus penetrans and Rhizoctonia fragariae in Strawberry Black Root Rot. J Nematol 35:17–22
- Larkin RP, Fravel DR (1999) Mechanisms of action and dose-response relationships governing biological control of Fusarium wilt of tomato by nonpathogenic Fusarium spp. Phytopathology 89:1152–1161
- Larkin RP, Hopkins DL, Martin FN (1996) Suppression of Fusarium wilt of watermelon by nonpathogenic Fusarium oxysporum and other microorganism recovered from a disease suppressive soil. Phytopathology 86:812–819
- Li X, Gao Y, Jian Q, Zhang Z, Liu S, Chen F, Zhang J (2016) Ferric reduction oxidase 2 gene from Pyrus betulifolia Bunge is regulated by iron deficiency and auxin. Can J Plant Sci 97:1–11
- Lievens B, Vaes K, Coosemans J, Ryckeboer J (2001) Systemic resistance induced in cucumber against Pythium root rot by source separated household waste and yard trimmings composts. Compost Sci Util 9:221–229
- Lima RSN, García-Tejero I, Lopes TS, Costa JM, Vaz M, Durán-Zuazo VH, Chaves M, Glenn DM, Campostrini E (2016) Linking thermal imaging to physiological indicators in Carica papaya L. under different watering regimes. Agric Water Manag 164:148–157
- Ling N, Huang Q, Guo S, Shen Q (2011) Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f. sp. niveum. Plant Soil 341:485–493
- Liu L, Kloepper JW, Tuzun S (1995) Induction of systemic resistance in cucumber against Fusarium wilt by plant growth-promoting rhizobacteria. Phytopathology 85:695–698
- Liu Y, Chen L, Wu G, Feng H, Zhang G, Shen Q, Zhang R (2017) Identification of root-secreted compounds involved in the communication between cucumber, the beneficial Bacillus amyloliquefaciens, and the soil-borne pathogen Fusarium oxysporum. Mol Plant-Microbe Interact 30:53–62
- Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
- Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol 48:395–417
- Martínez-Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CMJ, Van Wees SCM (2017) Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol 213:1363–1377
- Martinuz A, Schouten A, Sikora RA (2012) Systemically induced resistance and microbial competitive exclusion: implications on biological control. Phytopathology 102:260–266
- Martinuz A, Zewdu G, Ludwig N, Grundler F, Sikora RA, Schouten A (2015) The application of Arabidopsis thaliana in studying tripartite interactions among plants, beneficial fungal endophytes and biotrophic plant-parasitic nematodes. Planta 241:1015–1025
- McKenry MV, Anwar SA (2007) Virulence of Meloidogyne spp. and induced resistance in grape rootstocks. J Nematol 39:50
- Medeiros HA, Araújo Filho JV, Freitas LG, Castillo P, Rubio MB, Hermosa R, Monte E (2017) Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Sci Rep 7:40216
- Mishra AK, Morang P, Deka M, Kumar SN, Kumar BD (2014) Plant growth-promoting rhizobacterial strain-mediated induced systemic resistance in Tea (Camellia sinensis (L.) O. Kuntze) through defense-related enzymes against brown root rot and charcoal stump rot. Appl Biochem Biotechnol 174:506–521
- Monfort E, Lopez-Llorca LV, Jansson HB, Salinas J, Park JO, Sivasithamparam K (2005) Colonisation of seminal roots of wheat and barley by egg-parasitic nematophagous fungi and their effects on Gaeumannomyces graminis var. tritici and development of root-rot. Soil Biol Biochem 37:1229–1235
- Moreno CA, Castillo F, González A, Bernal D, Jaimes Y, Chaparro M, González C, Rodriguez F, Restrepo S, Cotes AM (2009) Biological and molecular characterization of the response of tomato plants treated with Trichoderma koningiopsis. Physiol Mol Plant Pathol 74:111–120
- Pantelides IS, Tjamos SE, Striglis IA, Chatzipavlidis I, Paplomatas EJ (2009) Mode of action of a non-pathogenic Fusarium oxysporum strain against Verticillium dahliae using Real Time QPCR analysis and biomarker transformation. Biol Control 50:30–36
- Papasotiriou FG, Varypatakis KG, Christofi N, Tjamos SE, Paplomatas EJ (2013) Olive mill wastes: a source of resistance for plants against Verticillium dahliae and a reservoir of biocontrol agents. Biol Control 67:51–60
- Pedroche NB, Villanueva LM, De Waele D (2009) Management of root-knot nematode, Meloidogyne incognita in carrot. Commun Agric Appl Biol Sci 74:605–615
- Piśkiewicz AM, Duyts H, Van Der Putten WH (2009) Soil microorganisms in coastal foredunes control the ectoparasitic root-feeding nematode Tylenchorhynchus ventralis by local interactions. Funct Ecol 23:621–626
- Postma J, Luttikholt AJ (1996) Colonization of carnation stems by a nonpathogenic isolate of Fusarium oxysporum and its effect on Fusarium oxysporum f. sp. dianthi. Can J Bot 74:1841–1851
- Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534
- Rao MS, Reddy PP, Nagesh M (1998) Evaluation of plant based formulations of Trichoderma harzianum for management of Meloidogyne incognita on egg plant. Nematol Mediterr 26:59–62
- Redwan M, Spinelli F, Marti L, Bazihizina N, Azzarello E, Mancuso S, Masi E (2017) Investigation of root signaling under heterogeneous salt stress: a case study for Cucumis sativus L. Environ Exp Bot 143:20–28
- Reitz M, Rudolph K, Schröder I, Hoffmann-Hergarten S, Hallmann J, Sikora RA (2000) Lipopolysaccharides of Rhizobium etli strain G12 act in potato roots as an inducing agent of systemic resistance to infection by the cyst nematode Globodera pallida. Appl Environ Microbiol 66:3515–3518
- Rubio MB, Quijada NM, Perez E, Dominguez S, Monte E, Hermosa R (2014) Identifying beneficial qualities of Trichoderma parareesei for plants. Appl Environ Microbiol 80:1864–1873
- Rubio MB, Hermosa R, Vicente R, Gómez-Acosta FA, Morcuende R, Monte E, Bettiol W (2017) The combination of Trichoderma harzianum and chemical fertilization leads to the deregulation of phytohormone networking, preventing the adaptive responses of tomato plants to salt stress. Front Plant Sci 8:294
- Sánchez-Hermosilla J, Rincón VJ, Páez F, Fernández M (2012) Comparative spray deposits by manually pulled trolley sprayer and a spray gun in greenhouse tomato crops. Crop Prot 31:119–124
- Sargent L, Huang SZ, Rolfe BG, Djordjevic MA (1987) Split-root assays using Trifolium subterraneum show that Rhizobium infection induces a systemic response that can inhibit nodulation of another invasive Rhizobium strain. Appl Environ Microbiol 53:1611–1619
- Selim ME, Mahdy ME, Sorial ME, Dababat AA, Sikora RA (2014) Biological and chemical dependent systemic resistance and their significance for the control of root-knot nematodes. Nematology 16:917–927
- Shanmugam V, Kanoujia N (2011) Biological management of vascular wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici by plant growth-promoting rhizobacterial mixture. Biol Control 57:85–93
- Sharon E, Bar-Eyal M, Chet I, Herrera-Estrella A, Kleifeld O, Spiegel Y (2001) Biocontrol of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology 91:687–693
- Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43
- Siddiqui IA, Shaukat SS (2002a) Rhizobacteria-mediated Induction of Systemic Resistance (ISR) in Tomato against Meloidogyne javanica. J Phytopathol 150:469–473
- Siddiqui IA, Shaukat SS (2002b) Resistance against the damping-off fungus Rhizoctonia solani systemically induced by the plant-growth-promoting rhizobacteria Pseudomonas aeruginosa (IE-6S+) and P. fluorescens (CHA0). J Phytopathol 150:500–506
- Siddiqui IA, Shaukat SS (2004) Systemic resistance in tomato induced by biocontrol bacteria against the root-knot nematode, Meloidogyne javanica is independent of salicylic acid production. J Phytopathol 152:48–54
- Silva AR, Araújo JV, Braga FR, Frassy LM, Tavela AO, Carvalho RO, Castejon FV (2009) Biological control of sheep gastrointestinal nematodiasis in a tropical region of the southeast of Brazil with the nematode predatory fungi Duddingtonia flagrans and Monacrosporium thaumasium. Parasitol Res 105:1707–1713
- Sokhandani Z, Moosavi MR, Basirnia T (2016) Optimum concentrations of Trichoderma longibrachiatum and cadusafos for controlling Meloidogyne javanica on zucchini plants. J Nematol 48:54–63
- Soler A, Marie-Alphonsine PA, Corbion C, Quénéhervé P (2013) Differential response of two pineapple cultivars (Ananas comosus (L.) Merr.) to SAR and ISR inducers against the nematode Rotylenchulus reniformis. Crop Prot 54:48–54
- Tian F, Wang Y, Zhu X, Chen L, Duan Y (2014) Effect of Sinorhizobium fredii strain Sneb183 on the biological control of soybean cyst nematode in soybean. J Basic Microbiol 54:1258–1263
- Umesh KC, Ferris H, Bayer DE (1994) Competition between the plant-parasitic nematodes Pratylenchus neglectus and Meloidogyne chitwoodi. J Nematol 26:286–295
- Vierheilig H, Garcia-Garrido JM, Wyss U, Piché Y (2000) Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem 32:589–595
- Vierheilig H, Lerat S, Piché Y (2003) Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 13:167–170
- Vos CM, Tesfahun AN, Panis B, De Waele D, Elsen A (2012) Arbuscular mycorrhizal fungi induce systemic resistance in tomato against the sedentary nematode Meloidogyne incognita and the migratory nematode Pratylenchus penetrans. Appl Soil Ecol 61:1–6
- Vu T, Hauschild R, Sikora RA (2006) Fusarium oxysporum endophytes induced systemic resistance against Radopholus similis on banana. Nematology 8:847–852
- Xin J, Dai H, Huang B (2017) Assessing the roles of roots and shoots in the accumulation of cadmium in two sweet potato cultivars using split-root and reciprocal grafting systems. Plant Soil 412:413–424
- Yogev A, Raviv M, Hadar Y, Cohen R, Wolf S, Gil L, Katan J (2010) Induced resistance as a putative component of compost suppressiveness. Biol Control 54:46–51
- 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
- Zhang G, Raza W, Wang X, Ran W, Shen Q (2012) Systemic modification of cotton root exudates induced by arbuscular mycorrhizal fungi and Bacillus vallismortis HJ-5 and their effects on Verticillium wilt disease. Appl Soil Ecol 61:85–91
- Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. J Phytopathol 152:537–542