Skip to main content

Belowground Defence Strategies Against Verticillium Pathogens

  • Chapter
  • First Online:
Belowground Defence Strategies in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Plant pathogenic Verticillium species cause vascular infections in many dicot species and show a complex interaction with their hosts. The soil-borne fungi start infections on roots, traverse the root cortex to enter the xylem and spread systemically inside the vasculature. The disease symptoms include wilting, leaf necrosis, stem discoloration and/or premature senescence. Finally the host plant is systemically colonized, and resting structures are formed in the infected tissue. Control of this disease relies primarily on quantitative host resistance, and many studies have built a multifaceted picture of the many factors that are involved in defence on different levels. Once the first major barrier—the endodermis—has been overcome, defence reactions are primarily targeting the fungus in the vascular system and involve many components that have been described for pathogen-associated molecular pattern (PAMP)-triggered but also for effector-triggered immunity. Results from the recently described interaction between Verticillium longisporum and Brassicaceae hosts are reviewed more comprehensively, and own data on the gene expression pattern characterizing the defence response against systemic colonization in Arabidopsis thaliana are presented. Gene expression analysis in line with contrasting reactions revealed the absence of multiple defence gene induction in the susceptible line at the onset of systemic colonization. With respect to the available knowledge on Verticillium and its interactions, it should be possible to support the control of Verticillium by applying a plethora of science-based strategies that will more and more meet practical demands.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Angelopoulou DJ, Naska EJ, Paplomatas EJ et al (2014) Biological control agents (BCAs) of Verticillium wilt: influence of application rates and delivery method on plant protection triggering of host defence mechanisms and rhizosphere populations of BCAs. Plant Pathol 63:1062–1069

    Article  Google Scholar 

  • Aranda S, Montes-Borrego M, Jiménez-Díaz RM et al (2011) Microbial communities associated with the root system of wild olives (Olea europaea L subsp europaea var sylvestris) are good reservoirs of bacteria with antagonistic potential against Verticillium dahliae. Plant Soil 343:329–345

    Article  CAS  Google Scholar 

  • Arias-Calderón R, León L, Bejarano-Alcázar J et al (2015) Resistance to Verticillium wilt in olive progenies from open-pollination. Sci Hortic 185:34–42

    Article  Google Scholar 

  • Arshad M, Frankenberger WT (1993) Microbial production of plant growth regulators. In: Blaine F, Metting JR (eds) Soil microbial ecology. Marcel and Dekker, New York, pp 307–347

    Google Scholar 

  • Báidez AG, Gómez P, Del Río JA et al (2007) Dysfunctionality of the xylem in Olea europaea L plants associated with the infection process by Verticillium dahliae Kleb. Role of phenolic compounds in plant defense mechanism. J Agric Food Chem 55:3373–3377

    Article  PubMed  CAS  Google Scholar 

  • Bak S, Tax FE, Feldmann KA et al (2001) CYP83B1 a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:101–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beckman CH (2000) Phenolic-storing cells: keys to programmed cell death and periderm formation in wilt disease resistance and in general defence responses in plants? Physiol Mol Plant Pathol 57:101–110

    Article  CAS  Google Scholar 

  • Bednarek P, Piślewska-Bednarek M, Svatoš A et al (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defence. Science 323:101–106

    Article  CAS  PubMed  Google Scholar 

  • Benhamou N (1995) Ultrastructural and cytochemical aspects of the response of eggplant parenchyma cells in direct contact with Verticillium-infected xylem vessels. Physiol Mol Plant Pathol 46:321–338

    Article  Google Scholar 

  • Bishop CD, Cooper RM (1983) An ultrastructural study of root invasion in three vascular wilt diseases. Physiol Plant Pathol 22:15–27

    Article  Google Scholar 

  • Blasingame D, Patel MV (2005) Cotton disease loss estimate committee report. In: Proceedings of Beltwide cotton conference, pp 259–262

    Google Scholar 

  • Bolek Y, El-Zik KM, Pepper AE et al (2005) Mapping of verticillium wilt resistance genes in cotton. Plant Sci 168:1581–1590

    Article  CAS  Google Scholar 

  • Bonanomi G, Antignani V, Capodilupo M et al (2010) Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biol Biochem 42:136–144

    Article  CAS  Google Scholar 

  • Bowers JH, Nameth ST, Riedel RM et al (1996) Infection and colonization of potato roots by Verticillium dahliae as affected by Pratylenchus penetrans and P. crenatus. Phytopathology 86:614–621

    Article  Google Scholar 

  • Chai Y, Zhao L, Liao Z et al (2003) Molecular cloning of a potential Verticillium dahliae resistance gene SlVe 1 with multi-site polyadenylation from Solanum licopersicoides. DNA Seq 14:375–384

    Article  CAS  PubMed  Google Scholar 

  • Chen XY, Chen Y, Heinstein P et al (1995) Cloning expression and characterization of (+)-δ-cadinene synthase: a catalyst for cotton phytoalexin biosynthesis. Arch Biochem Biophys 324:255–266

    Article  CAS  PubMed  Google Scholar 

  • Chen JY, Huang JQ, Li NY et al (2015) Genome-wide analysis of the gene families of resistance gene analogues in cotton and their response to Verticillium wilt. BMC Plant Biol 15:148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cui Y, Bell AA, Joost O et al (2000) Expression of potential defense response genes in cotton. Physiol Mol Plant Pathol 56:25–31

    Article  CAS  Google Scholar 

  • Daayf F (2015) Verticillium wilts in crop plants: pathogen invasion and host defence responses. Can J Plant Pathol 37:8–20

    Article  CAS  Google Scholar 

  • De Coninck B, Timmermans P, Vos C et al (2015) What lies beneath: belowground defence strategies in plants. Trends Plant Sci 20:91–101

    Article  CAS  PubMed  Google Scholar 

  • de Jonge R, van Esse HP, Maruthachalam K et al (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109:5110–5115

    Article  PubMed  PubMed Central  Google Scholar 

  • de Jonge R, Bolton MD, Kombrink A et al (2013) Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res 23:1271–1282

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dixon GR, Pegg GF (1969) Hyphal lysis and tylose formation in tomato cultivars infected by Verticillium albo-atrum. Trans Br Mycol Soc 53:109–118

    Article  Google Scholar 

  • Dixon RA, Achnine L, Kota P et al (2002) The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 3:371–390

    Article  CAS  PubMed  Google Scholar 

  • Dong H, Cohen Y (2002) Dry mycelium of Penicillium chrysogenum induces resistance against Verticillium wilt and enhances growth of cotton plants. Phytoparasitica 30:147–157

    Article  Google Scholar 

  • Dunker S, Keunecke H, Steinbach P et al (2008) Impact of Verticillium longisporum on yield and morphology of winter oilseed rape (Brassica napus) in relation to systemic spread in the plant. J Phytopathol 156:698–707

    Article  Google Scholar 

  • Durrands PK, Cooper RM (1988) The role of pectinases in vascular wilt disease as determined by defined mutants of Verticillium albo-atrum. Physiol Mol Plant Pathol 32:363–371

    Article  Google Scholar 

  • El‐Bebany AF, Rampitsch C, Daayf F (2010) Proteomic analysis of the phytopathogenic soilborne fungus Verticillium dahliae reveals differential protein expression in isolates that differ in aggressiveness. Proteomics 10:289–303

    Article  PubMed  CAS  Google Scholar 

  • Ellendorff U, Fradin EF, de Jonge R et al (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J Exp Bot 60:591–602

    Article  CAS  PubMed  Google Scholar 

  • Eynck C, Koopmann B, Grunewaldt-Stoecker G et al (2007) Differential interactions of Verticillium longisporum and V. dahliae with Brassica napus detected with molecular and histological techniques. Eur J Plant Pathol 118:259–274

    Article  Google Scholar 

  • Eynck C, Koopmann B, Karlovsky P et al (2009) Internal resistance in winter oilseed rape inhibits systemic spread of the vascular pathogen Verticillium longisporum. Phytopathology 99:802–811

    Article  CAS  PubMed  Google Scholar 

  • Fei J, Chai Y, Wang J et al (2004) cDNA cloning and characterization of the Ve homologue gene StVe from Solanum torvum Swartz. DNA Seq 15:88–95

    Article  CAS  PubMed  Google Scholar 

  • Fradin EF, Thomma BP (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo‐atrum. Mol Plant Pathol 7:71–86

    Article  CAS  PubMed  Google Scholar 

  • Fradin EF, Zhang Z, Ayala JCJ et al (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150:320–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fradin EF, Abd-El-Haliem A, Masini L et al (2011) Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol 156:2255–2265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frerigmann H, Gigolashvili T (2014) MYB34, MYB51 and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana. Mol Plant 7:814–828

    Article  CAS  PubMed  Google Scholar 

  • Gao W, Long L, Zhu LF et al (2013) Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae. Mol Cell Proteomics 12:3690–3703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garmendia I, Aguirreolea J, Goicoechea N (2006) Defence-related enzymes in pepper roots during interactions with arbuscular mycorrhizal fungi and/or Verticillium dahliae. BioControl 51:293–310

    Article  CAS  Google Scholar 

  • Gayoso C, Pomar F, Novo-Uzal E et al (2010) The Ve-mediated resistance response of the tomato to Verticillium dahliae involves H2O2, peroxidase and lignins and drives PAL gene expression. BMC Plant Biol 10:232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gladders P (2009) Relevance of verticillium wilt (Verticillium longisporum) in winter oilseed rape in the UK. HGCA Res Rev 72

    Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Göre ME, Erdoğan O, Altin N et al (2011) Seed transmission of Verticillium wilt of cotton. Phytoparasitica 39:285–292

    Article  Google Scholar 

  • Goud JKC, Termorshuizen AJ, Blok WJ et al (2004) Long-term effect of biological soil disinfestation on Verticillium wilt. Plant Dis 88:688–694

    Article  Google Scholar 

  • Griffiths D (1971) The development of lignitubers in roots after infection by Verticillium dahliae Kleb. Can J Microbiol 17:441–444

    Article  CAS  PubMed  Google Scholar 

  • Häffner E, Karlovsky P, Diederichsen E (2010) Genetic and environmental control of the Verticillium syndrome in Arabidopsis thaliana. BMC Plant Biol 10:235

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Häffner E, Karlovsky P, Splivallo R et al (2014) ERECTA salicylic acid abscisic acid and jasmonic acid modulate quantitative disease resistance of Arabidopsis thaliana to Verticillium longisporum. BMC Plant Biol 14:85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Häffner E, Konietzki S, Diederichsen E (2015) Keeping Control: the role of senescence and development in plant pathogenesis and defence. Plants 4:449–488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333

    Article  CAS  PubMed  Google Scholar 

  • Han Q, Wu F, Wang X et al (2015) The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen‐associated molecular pattern‐triggered immunity. Environ Microbiol 17:1166–1188

    Article  CAS  PubMed  Google Scholar 

  • Hanson LE, Howell CR (2004) Elicitors of plant defense responses from biocontrol strains of Trichoderma virens. Phytopathology 94:171–176

    Article  CAS  PubMed  Google Scholar 

  • Heale JB, Karapapa VK (1999) The Verticillium threat to Canada’s major oilseed crop: canola. Can J Plant Pathol 21:1–7

    Article  Google Scholar 

  • Heinz R, Lee SW, Saparno A et al (1998) Cyclical systemic colonization in Verticillium-infected tomato. Physiol Mol Plant Pathol 52:385–396

    Article  Google Scholar 

  • Hoppenau CE, Tran VT, Kusch H et al (2014) Verticillium dahliae VdTHI4 involved in thiazole biosynthesis stress response and DNA repair functions is required for vascular disease induction in tomato. Environ Exp Bot 108:14–22

    Article  CAS  Google Scholar 

  • Huisman OC (1982) Interrelations of root growth dynamics to epidemiology of root-invading fungi. Annu Rev Phytopathol 20:303–327

    Article  Google Scholar 

  • Inderbitzin P, Subbarao KV (2014) Verticillium systematics and evolution: how confusion impedes Verticillium wilt management and how to resolve it. Phytopathology 104:564–574

    Article  PubMed  Google Scholar 

  • Inderbitzin P, Bostock RM, Davis RM et al (2011) Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium with the descriptions of five new species. PLoS One 6:e28341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iven T, König S, Singh S et al (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in Arabidopsis roots contributes to the defence against the fungal vascular pathogen Verticillium longisporum. Mol Plant 5:1389–1402

    Article  CAS  PubMed  Google Scholar 

  • Jakse J, Cerenak A, Radišek S et al (2013) Identification of quantitative trait loci for resistance to Verticillium wilt and yield parameters in hop (Humulus lupulus L). Theor Appl Genet 126:1431–1443

    Article  CAS  PubMed  Google Scholar 

  • James JT, Dubery IA (2001) Inhibition of polygalacturonase from Verticillium dahliae by a polygalacturonase inhibiting protein from cotton. Phytochemistry 57:149–156

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Díaz RM, Millar RL (1988) Sporulation on infected tissues and presence of airborne Verticillium albo‐atrum in alfalfa fields in New York. Plant Pathol 37:64–70

    Article  Google Scholar 

  • Joaquim TR, Rowe RC (1991) Vegetative compatibility and virulence of strains of Verticillium dahliae from soil and potato plants. Phytopathology 81:552–558

    Article  Google Scholar 

  • Johansson A, Staal J, Dixelius C (2006) Early responses in the Arabidopsis-Verticillium longisporum pathosystem are dependent on NDR1 JA-and ET-associated signals via cytosolic NPR1 and RFO1. Mol Plant Microbe Interact 19:958–969

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kamble A, Koopmann B, von Tiedemann A (2013) Induced resistance to Verticillium longisporum in Brassica napus by β‐aminobutyric acid. Plant Pathol 62:552–561

    Article  CAS  Google Scholar 

  • Karademir E, Karademir C, Ekinci R et al (2012) Effect of Verticillium dahliae Kleb on cotton yield and fiber technological properties. Int J Plant Prod 6:387–407

    Google Scholar 

  • Karagiannidis N, Bletsos F, Stavropoulos N (2002) Effect of Verticillium wilt (Verticillium dahliae Kleb) and mycorrhiza (Glomus mosseae) on root colonization, growth and nutrient uptake in tomato and eggplant seedlings. Sci Hortic 94:145–156

    Article  CAS  Google Scholar 

  • Karajeh MR (2006) Seed transmission of Verticillium dahliae in olive as detected by a highly sensitive nested PCR-based assay. Phytopathol Mediterr 45:5–23

    Google Scholar 

  • Karapapa VK, Bainbridge BW, Heale JB (1997) Morphological and molecular characterization of Verticillium longisporum comb. nov. pathogenic to oilseed rape. Mycol Res 101:1281–1294

    Article  Google Scholar 

  • Kawchuk LM, Hachey J, Lynch DR et al (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA 98:6511–6515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klosterman SJ, Atallah ZK, Vallad GE et al (2009) Diversity Pathogenicity and management of Verticillium species. Annu Rev Phytopathol 47:39–62

    Article  CAS  PubMed  Google Scholar 

  • König S, Feussner K, Kaever A et al (2014) Soluble phenylpropanoids are involved in the defence response of Arabidopsis against Verticillium longisporum. New Phytol 202:823–837

    Article  PubMed  CAS  Google Scholar 

  • Li C, He X, Luo X et al (2014) Cotton WRKY1 mediates the plant defense-to-development transition during infection of cotton by Verticillium dahliae by activating JASMONATE ZIM-DOMAIN1 expression. Plant Physiol 166:2179–2194

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu SY, Chen JY, Wang JL et al (2013) Molecular characterization and functional analysis of a specific secreted protein from highly virulent defoliating Verticillium dahliae. Gene 529:307–316

    Article  CAS  PubMed  Google Scholar 

  • López-Escudero FJ, Mercado-Blanco J (2011) Verticillium wilt of olive: a case study to implement an integrated strategy to control a soil-borne pathogen. Plant Soil 344:1–50

    Article  CAS  Google Scholar 

  • Luo X, Xie C, Dong J (2014) Interactions between Verticillium dahliae and its host: vegetative growth, pathogenicity, plant immunity. Appl Microbiol Biotechnol 98:6921–6932

    Article  CAS  PubMed  Google Scholar 

  • Mace ME, Stipanovic RD, Bell AA (1985) Toxicity and role of terpenoid phytoalexins in Verticillium wilt resistance in cotton. Physiol Plant Pathol 26:209–218

    Article  CAS  Google Scholar 

  • Mandelc S, Timperman I, Radišek S et al (2013) Comparative proteomic profiling in compatible and incompatible interactions between hop roots and Verticillium albo-atrum. Plant Physiol Biochem 68:23–31

    Article  CAS  PubMed  Google Scholar 

  • Markakis EA, Tjamos SE, Antoniou PP et al (2010) Phenolic responses of resistant and susceptible olive cultivars induced by defoliating and nondefoliating Verticillium dahliae pathotypes. Plant Dis 94:1156–1162

    Article  CAS  Google Scholar 

  • Mercado-Blanco J, Rodríguez-Jurado D, Pérez-Artés E et al (2002) Detection of the defoliating pathotype of Verticillium dahliae in infected olive plants by nested PCR. Eur J Plant Pathol 108:1–13

    Article  CAS  Google Scholar 

  • Mercado-Blanco J, Collado-Romero M, Parrilla-Araujo S et al (2003) Quantitative monitoring of colonization of olive genotypes by Verticillium dahliae pathotypes with real-time polymerase chain reaction. Physiol Mol Plant Pathol 63:91–105

    Article  CAS  Google Scholar 

  • Mercado-Blanco J, Rodrıguez-Jurado D, Hervás A et al (2004) Suppression of Verticillium wilt in olive planting stocks by root-associated fluorescent Pseudomonas spp. Biol Control 30:474–486

    Article  Google Scholar 

  • Millet YA, Danna CH, Clay NK et al (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mol L (1995) Formation of microsclerotia of Verticillium dahliae on various crops. NJAS Wageningen J Life Sci 43:205–215

    Google Scholar 

  • Nagano AJ, Fukao Y, Fujiwara M et al (2008) Antagonistic jacalin-related lectins regulate the size of ER body-type β-glucosidase complexes in Arabidopsis thaliana. Plant Cell Physiol 49:969–980

    Article  CAS  PubMed  Google Scholar 

  • Narisawa K, Kawamata H, Currah RS et al (2002) Suppression of Verticillium wilt in eggplant by some fungal root endophytes. Eur J Plant Pathol 108:103–109

    Article  Google Scholar 

  • Narisawa K, Usuki F, Hashiba T (2004) Control of Verticillium yellows in Chinese cabbage by the dark septate endophytic fungus LtVB3. Phytopathology 94:412–418

    Article  CAS  PubMed  Google Scholar 

  • Nejad P, Johnson PA (2000) Endophytic bacteria induce growth promotion and wilt disease suppression in oilseed rape and tomato. Biol Control 18:208–215

    Article  Google Scholar 

  • Novakazi F, Inderbitzin P, Sandoya G et al (2015) The three lineages of the diploid hybrid verticillium longisporum differ in virulence and pathogenicity. Phytopathology 105:662–673

    Article  PubMed  Google Scholar 

  • Obermeier C, Hossain MA, Snowdon R et al (2013) Genetic analysis of phenylpropanoid metabolites associated with resistance against Verticillium longisporum in Brassica napus. Mol Breed 31:347–361

    Article  CAS  Google Scholar 

  • Olsson S, Nordbring-Hertz B (1985) Microsclerotial germination of Verticillium dahliae as affected by rape rhizosphere. FEMS Microbiol Ecol 31:293–299

    Article  Google Scholar 

  • Pegg GF (1974) Verticillium diseases. Rev Plant Pathol 53:82

    Google Scholar 

  • Pegg GF, Brady BL (2002) Verticillium wilts. CABI, Wallingford

    Book  Google Scholar 

  • Pham GH, Singh A, Malla R et al (2008) Interaction of Piriformospora indica with diverse microorganisms and plants. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Heidelberg, pp 237–265

    Chapter  Google Scholar 

  • Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745–760

    Article  CAS  PubMed  Google Scholar 

  • Ralhan A, Schöttle S, Thurow C et al (2012) The vascular pathogen Verticillium longisporum requires a jasmonic acid-independent COI1 function in roots to elicit disease symptoms in Arabidopsis shoots. Plant Physiol 159:1192–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ratzinger A, Riediger N, von Tiedemann A et al (2009) Salicylic acid and salicylic acid glucoside in xylem sap of Brassica napus infected with Verticillium longisporum. J Plant Res 122:571–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reusche M, Thole K, Janz D et al (2012) Verticillium infection triggers VASCULAR-RELATED NAC DOMAIN7-dependent de novo xylem formation and enhances drought tolerance in Arabidopsis. Plant Cell 24:3823–3837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reusche M, Truskina J, Thole K et al (2014) Infections with the vascular pathogens Verticillium longisporum and Verticillium dahliae induce distinct disease symptoms and differentially affect drought stress tolerance of Arabidopsis thaliana. Environ Exp Bot 108:23–37

    Article  Google Scholar 

  • Robb J (2007) Verticillium tolerance: resistance susceptibility or mutualism? Botany 85:903–910

    Google Scholar 

  • Robb J, Brisson JD, Busch L et al (1979) Ultrastructure of wilt syndrome caused by Verticillium dahliae. VII Correlated light and transmission electron microscope identification of vessel coatings and tyloses. Can J Bot 57:822–834

    Article  Google Scholar 

  • Robb J, Lee B, Nazar RN (2007) Gene suppression in a tolerant tomato-vascular pathogen interaction. Planta 226:299–309

    Article  CAS  PubMed  Google Scholar 

  • Robb J, Shittu H, Soman KV et al (2012) Arsenal of elevated defense proteins fails to protect tomato against Verticillium dahliae. Planta 236:623–633

    Article  CAS  PubMed  Google Scholar 

  • Roos J, Bejai S, Oide S et al (2014) RabGAP22 is required for defence to the vascular pathogen Verticillium longisporum and contributes to stomata immunity. PLoS One 9:e88187

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63

    Article  CAS  PubMed  Google Scholar 

  • Rygulla W, Snowdon RJ, Friedt W et al (2008) Identification of quantitative trait loci for resistance against Verticillium longisporum in oilseed rape (Brassica napus). Phytopathology 98:215–221

    Article  CAS  PubMed  Google Scholar 

  • Sacristán S, García‐Arenal F (2008) The evolution of virulence and pathogenicity in plant pathogen populations. Mol Plant Pathol 9:369–384

    Article  PubMed  Google Scholar 

  • Scher FM, Baker R (1982) Effect of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness to Fusarium wilt pathogens. Phytopathology 72:1567–1573

    Article  CAS  Google Scholar 

  • Schnathorst WC (1981) Life-cycle and epidemiology of Verticillium. In: Mace ME, Bel AA, Beckman CH (eds) Fungal wilt diseases of plants. Academic, New York, pp 81–108

    Chapter  Google Scholar 

  • Schreiber LR, Green RJ (1963) Effect of root exudates on germination of conidia and microsclerotia of Verticillium albo-atrum inhibited by soil fungistatic principle. Phytopathology 53:260–264

    Google Scholar 

  • Shen D, Suhrkamp I, Wang Y et al (2014) Identification and characterization of microRNAs in oilseed rape (Brassica napus) responsive to infection with the pathogenic fungus Verticillium longisporum using Brassica AA (Brassica rapa) and CC (Brassica oleracea) as reference genomes. New Phytol 204:577–594

    Article  CAS  PubMed  Google Scholar 

  • Shittu HO, Castroverde DC, Nazar RN et al (2009) Plant-endophyte interplay protects tomato against a virulent Verticillium. Planta 229:415–426

    Article  CAS  PubMed  Google Scholar 

  • Simko I, Costanzo S, Haynes KG et al (2004) Linkage disequilibrium mapping of a Verticillium dahliae resistance quantitative trait locus in tetraploid potato (Solanum tuberosum) through a candidate gene approach. Theor Appl Genet 108:217–224

    Article  CAS  PubMed  Google Scholar 

  • Smit F, Dubery IA (1997) Cell wall reinforcement in cotton hypocotyls in response to a Verticillium dahliae elicitor. Phytochemistry 44:811–815

    Article  CAS  Google Scholar 

  • Spek J (1973) Seed transmission of Verticillium dahliae. Mededelingen van de Faculteit Landbouwwetenschappen Rijksuniversiteit Gent 38:1427–1434

    Google Scholar 

  • Sun C, Shao Y, Vahabi K et al (2014) The beneficial fungus Piriformospora indica protects Arabidopsis from Verticillium dahliae infection by downregulation plant defense responses. BMC Plant Biol 14:268

    Article  PubMed  PubMed Central  Google Scholar 

  • Tai HH, Goyer C, De Koeyer D et al (2013) Decreased defense gene expression in tolerance versus resistance to Verticillium dahliae in potato. Funct Integr Genomics 13:367–378

    Article  CAS  PubMed  Google Scholar 

  • Talboys PW (1958) Association of tylosis and hyperplasia of the xylem with vascular invasion of the hop by Verticillium albo-atrum. Trans Br Mycol Soc 41:249–260

    Article  Google Scholar 

  • Talboys PW (1972) Resistance to vascular wilt fungi. Proc R Soc Lond B Biol Sci 181:319–332

    Article  CAS  Google Scholar 

  • Thatcher LF, Manners JM, Kazan K (2009) Fusarium oxysporum hijacks COI1‐mediated jasmonate signalling to promote disease development in Arabidopsis. Plant J 58:927–939

    Article  CAS  PubMed  Google Scholar 

  • The Arabidopsis information resource (TAIR). http://www.arabidopsis.org. Accessed 21 Nov 2015

  • Thimm O, Bläsing O, Gibon Y et al (2004) MAPMAN: a user‐driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Thomma BP, Nürnberger T, Joosten MH (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timpner C, Braus-Stromeyer SA, Tran VT et al (2013) The Cpc1 regulator of the cross-pathway control of amino acid biosynthesis is required for pathogenicity of the vascular pathogen Verticillium longisporum. Mol Plant Microbe Interact 26:1312–1324

    Article  CAS  PubMed  Google Scholar 

  • Tischner R, Koltermann M, Hesse H et al (2010) Early responses of Arabidopsis thaliana to infection by Verticillium longisporum. Physiol Mol Plant Pathol 74:419–427

    Article  CAS  Google Scholar 

  • Tjamos SE, Flemetakis E, Paplomatas EJ et al (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18:555–561

    Article  CAS  PubMed  Google Scholar 

  • Uppal AK, El Hadrami A, Adam LR et al (2008) Biological control of potato Verticillium wilt under controlled and field conditions using selected bacterial antagonists and plant extracts. Biol Control 44:90–100

    Article  Google Scholar 

  • Vallad GE, Subbarao KV (2008) Colonization of resistant and susceptible lettuce cultivars by a green fluorescent protein-tagged isolate of Verticillium dahliae. Phytopathology 98:871–885

    Article  CAS  PubMed  Google Scholar 

  • Vallad GE, Bhat RG, Koike ST et al (2005) Weedborne reservoirs and seed transmission of Verticillium dahliae in lettuce. Plant Dis 89:317–324

    Article  Google Scholar 

  • Van Etten HD, Mansfield JW, Bailey JA et al (1994) Two classes of plant antibiotics: phytoalexins versus “phytoanticipins”. Plant Cell 6:1191

    Article  Google Scholar 

  • Van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defence-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  CAS  Google Scholar 

  • Varma A, Verma S, Sahay N et al (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Veloso J, Díaz J (2012) Fusarium oxysporum Fo47 confers protection to pepper plants against Verticillium dahliae and Phytophthora capsici and induces the expression of defence genes. Plant Pathol 61:281–288

    Article  CAS  Google Scholar 

  • Veronese P, Narasimhan ML, Stevenson RA et al (2003) Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. Plant J 35:574–587

    Article  CAS  PubMed  Google Scholar 

  • Vining K, Davis T (2009) Isolation of a Ve homolog mVe1 and its relationship to Verticillium wilt resistance in Mentha longifolia (L) Huds. Mol Genet Genomics 282:173–184

    Article  CAS  PubMed  Google Scholar 

  • Voinnet O (2008) Post-transcriptional RNA silencing in plant–microbe interactions: a touch of robustness and versatility. Curr Opin Plant Biol 11:464–470

    Article  CAS  PubMed  Google Scholar 

  • Wang JY, Cai Y, Gou JY et al (2004) VdNEP an elicitor from Verticillium dahliae induces cotton plant wilting. Appl Environ Microbiol 70:4989–4995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang FX, Ma YP, Yang CL et al (2011) Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae. Proteomics 11:4296–4309

    Article  CAS  PubMed  Google Scholar 

  • Weiberg A, Wang M, Lin FM et al (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G et al (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm S (1955) Longevity of the Verticillium wilt fungus in the laboratory and field. Phytopathology 45:180–181

    Google Scholar 

  • Witzel K, Hanschen FS, Schreiner M et al (2013) Verticillium suppression is associated with the glucosinolate composition of Arabidopsis thaliana leaves. PLoS One 8:e71877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Witzel K, Hanschen FS, Klopsch R et al (2015) Verticillium longisporum infection induces organ-specific glucosinolate degradation in Arabidopsis thaliana. Front Plant Sci 6:508

    PubMed  PubMed Central  Google Scholar 

  • Xu L, Zhu L, Tu L et al (2011) Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-seq-dependent transcriptional analysis and histochemistry. J Exp Bot 62:5607–5621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu L, Zhang W, He X et al (2014) Functional characterization of cotton genes responsive to Verticillium dahliae through bioinformatics and reverse genetics strategies. J Exp Bot 65:6679–6692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadeta KA, Thomma BP (2013) The xylem as battleground for plant hosts and vascular wilt pathogens. Front Plant Sci 4:97

    PubMed  PubMed Central  Google Scholar 

  • Yang Y, Ling X, Chen T et al (2014) A Cotton Gbvdr5 gene encoding a leucine-rich-repeat receptor-like protein confers resistance to Verticillium dahliae in transgenic Arabidopsis and Upland Cotton. Plant Mol Biol Rep. doi:10.1007/s11105-014-0810-5

    Google Scholar 

  • Yang CL, Liang S, Wang HY et al (2015a) Cotton major latex protein 28 functions as a positive regulator of the ethylene responsive factor 6 in defense against Verticillium dahliae. Mol Plant 8:399–411

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Mu X, Liu C et al (2015b) Overexpression of potato miR482e enhanced plant sensitivity to Verticillium dahliae infection. J Integr Plant Biol 57(12):1078–1088. doi:10.1111/jipb.12348

    Article  CAS  PubMed  Google Scholar 

  • Yao LL, Zhou Q, Pei BL et al (2011) Hydrogen peroxide modulates the dynamic microtubule cytoskeleton during the defence responses to Verticillium dahliae toxins in Arabidopsis. Plant Cell Environ 34:1586–1598

    Article  CAS  PubMed  Google Scholar 

  • Yin Z, Li Y, Han X et al (2012) Genome-wide profiling of miRNAs and other small non-coding RNAs in the Verticillium dahliae-inoculated cotton roots. PLoS One 7:e35765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan HY, Yao LL, Jia ZQ et al (2006) Verticillium dahliae toxin induced alterations of cytoskeletons and nucleoli in Arabidopsis thaliana suspension cells. Protoplasma 229:75–82

    Article  CAS  PubMed  Google Scholar 

  • Zeise K, von Tiedemann A (2002) Host specialization among vegetative compatibility groups of Verticillium dahliae in relation to Verticillium longisporum. J Phytopathol 150:112–119

    Article  Google Scholar 

  • Zhang Y, Wang X, Yang S et al (2011) Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbadense and functional analysis in Arabidopsis thaliana. Plant Cell Rep 30:2085–2096

    Article  CAS  PubMed  Google Scholar 

  • Zhang WW, Wang SZ, Liu K et al (2012a) Comparative expression analysis in susceptible and resistant Gossypium hirsutum responding to Verticillium dahliae infection by cDNA-AFLP. Physiol Mol Plant Pathol 80:50–57

    Article  CAS  Google Scholar 

  • Zhang WW, Jian GL, Jiang TF et al (2012b) Cotton gene expression profiles in resistant Gossypium hirsutum cv. Zhongzhimian KV1 responding to Verticillium dahliae strain V991 infection. Mol Biol Rep 39:9765–9774

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Yang Y, Chen T et al (2012c) Island cotton Gbve1 gene encoding a receptor-like protein confers resistance to both defoliating and non-defoliating isolates of Verticillium dahliae. PLoS One 7:e51091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Wang XF, Ding ZG et al (2013a) Transcriptome profiling of Gossypium barbadense inoculated with Verticillium dahliae provides a resource for cotton improvement. BMC Genomics 14:637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Fradin E, de Jonge R et al (2013b) Optimized agroinfiltration and virus-induced gene silencing to study Ve1-mediated Verticillium resistance in tobacco. Mol Plant Microbe Interact 26:182–190

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, van Esse HP, Damme M et al (2013c) Ve1‐mediated resistance against Verticillium does not involve a hypersensitive response in Arabidopsis. Mol Plant Pathol 14:719–727

    Article  CAS  PubMed  Google Scholar 

  • Zheng Z, Qamar SA, Chen Z et al (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Hu Q, Johansson A et al (2006) Verticillium longisporum and V dahliae: infection and disease in Brassica napus. Plant Pathol 55:137–144

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Sophia Harrand and Rebecca Werner for the excellent technical assistance. Funding from German Research Foundation (DFG, DI1502/3-1 grant) and the breeding company NPZ Norddeutsche Pflanzenzucht Hans-Georg Lembke KG is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elke Diederichsen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Häffner, E., Diederichsen, E. (2016). Belowground Defence Strategies Against Verticillium Pathogens. In: Vos, C., Kazan, K. (eds) Belowground Defence Strategies in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-42319-7_6

Download citation

Publish with us

Policies and ethics