Evaluation of pathogenicity, systemic colonisation, and host range of Verticillium alfalfae in a greenhouse
Fang Li
A and Yanzhong Li A B
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Ministry of Agriculture and Rural Affairs; State Key Laboratory of Grassland Agro-ecosystems; Engineering Research Centre of Grassland Industry, Ministry of Education; College of Pastoral Agriculture Science and Technology, Lanzhou University; Lanzhou 730020, China.
B Corresponding author. Email: liyzh@lzu.edu.cn
Crop and Pasture Science 72(5) 383-392 https://doi.org/10.1071/CP20449
Submitted: 6 November 2020 Accepted: 8 March 2021 Published: 26 May 2021
Abstract
Verticillium wilt of alfalfa (Medicago sativa) is a widespread and destructive disease caused by the soil-borne fungal pathogen Verticillium alfalfae (formerly V. albo-atrum before 2011). Owing to an inadequate understanding of the pathogenicity, systemic colonisation, and host range of V. alfalfae, it has been challenging to develop an effective control measure against this disease. In the present study, seven inoculation methods, including seed inoculation, leaf spraying (LS), fungal plugs placed on leaves (FP), stem injection (SI), root dipping (RD), root injuring and dipping (RI), and watering conidia suspension into soil (WI) were used to analyse the pathogenicity and systemic colonisation of V. alfalfae on alfalfa. The typical verticillium wilt symptoms including V-shaped necrosis of leaves and leaf wilting were observed in alfalfa plants with all inoculation methods. The shortest incubation period (9 days) was observed with stem injection and the longest (40 days) with root dipping. Alfalfa plants inoculated by stem injection showed the highest disease incidence (91%), disease index (65%), and percentage of infected plants (80%), which resulted in the highest shoot biomass loss rate (34%). However, the plants inoculated by fungal plugs showed the lowest disease index (4%), percentage of infected plants (10%), and root biomass loss rate (2%). Further, the stem injection method was used to assess the host range of V. alfalfae on seven non-alfalfa plant species including erect milkvetch, sainfoin, common vetch, sunflower, potato, cotton, and bluish dogbane. The artificial inoculation of V. alfalfae by stem injection successfully infected these plants, with disease incidence ranged from 13 to 100% and disease index ranged from 10 to 69. This indicates that host range of V. alfalfae is not only alfalfa, but also other plant species.
Keywords: alfalfa, forage yield, host range, inoculation method, pathogenicity, systemic colonisation, Verticillium alfalfa, verticillium wilt.
References
Atibalentja N, Eastburn DM (1997) Evaluation of inoculation methods for screening horseradish cultivars for resistance to Verticillium dahliae. Plant Disease 81, 356–362.| Evaluation of inoculation methods for screening horseradish cultivars for resistance to Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar | 30861815PubMed |
Barbara DJ, Clewes E (2003) Plant pathogenic Verticillium species: how many of them are there? Molecular Plant Pathology 4, 297–305.
| Plant pathogenic Verticillium species: how many of them are there?Crossref | GoogleScholarGoogle Scholar | 20569390PubMed |
Bergstrom GC (1984) ‘Verticillium wilt of alfalfa.’ (Cornell University: Ithaca, NY, USA)
Bibi N, Zhang GX, Li F, Fan K, Yuan SN, Wang XD (2013) Utilization of Vd toxin for rapid screening of cotton germplasm against Verticillium dahliae. Pakistan Journal of Botany 45, 2157–2162.
Bibi N, Li F, Ahmed IM, Fan K, Yuan SN, Wang XD (2017) Impact of Verticillium dahliae toxin on morphogenetic, physiological and biochemical characteristics of upland cotton. Pakistan Journal of Botany 49, 191–199.
Busch LV, Christie BR, Smith EA, Boland G (1985) Testing alfalfa cultivars for resistance to an alfalfa strain of Verticillium albo-atrum. Canadian Journal of Plant Pathology 7, 203–205.
| Testing alfalfa cultivars for resistance to an alfalfa strain of Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Calpas JT, Rahe JE (1995) Distribution of Verticillium albo-atrum in the root systems of resistant and susceptible alfalfa plants. Canadian Journal of Plant Pathology 17, 240–246.
| Distribution of Verticillium albo-atrum in the root systems of resistant and susceptible alfalfa plants.Crossref | GoogleScholarGoogle Scholar |
Correll JC, Gordon TR, McCain AH (1988) Vegetative compatibility and pathogenicity of Verticillium albo-atrum. Phytopathology 78, 1017–1021.
| Vegetative compatibility and pathogenicity of Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Erdoğan O, Göre ME, Özbek N (2012) Effects of green manure applications in the control of wilt disease (Verticillium dahliae) and yield on organic cotton production. Bitki Koruma Bulteni 52, 81–91.
Flood J, Milton JM (1982) Studies on the incompatible and compatible interactions between lucerne leaves and Verticillium albo-atrum. Physiological Plant Pathology 21, 97–104.
| Studies on the incompatible and compatible interactions between lucerne leaves and Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Flood J, Isaac I, Milton JM (1978) Reactions of some cultivars of lucerne to various isolates of Verticillium albo-atrum. Plant Pathology 27, 166–169.
| Reactions of some cultivars of lucerne to various isolates of Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Gómez-Gálvez FJ, Vega-Macías V, Hidalgo-Moya JC, Hidalgo-Moyab JJ, Rodríguez-Jurado D (2020) Application to soil of disinfectants through irrigation reduces Verticillium dahliae in the soil and verticillium wilt of olive. Plant Pathology 69, 272–283.
| Application to soil of disinfectants through irrigation reduces Verticillium dahliae in the soil and verticillium wilt of olive.Crossref | GoogleScholarGoogle Scholar |
Gómez-Vázquez J, Aguilera-Lirola A, Martín-Bretones G (2020) First report of verticillium wilt on eggplant in Almería Province, Spain. Plant Disease 104, 3260
| First report of verticillium wilt on eggplant in Almería Province, Spain.Crossref | GoogleScholarGoogle Scholar |
Grau CR, Nygaard SL, Arny DC, Delwiche PA (1991) Comparison of methods to evaluate alfalfa cultivars for reaction to Verticillium albo-atrum. Plant Disease 75, 82–85.
| Comparison of methods to evaluate alfalfa cultivars for reaction to Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Guo T, Bai J, Wang JG (2018) Research on the present situation and countermeasures of alfalfa grass industry in China. Chinese Journal of Grassland 4, 111–115.
Hampton RE, Wullschleger SD, Oosterhuis DM (1990) Impact of Verticillium wilt on net photosynthesis, respiration and photorespiration in field-grown cotton (Gossypium hirsutum). Physiological and Molecular Plant Pathology 37, 271–280.
| Impact of Verticillium wilt on net photosynthesis, respiration and photorespiration in field-grown cotton (Gossypium hirsutum).Crossref | GoogleScholarGoogle Scholar |
Heale JB, Isaac I (1963) Wilt of lucerne caused by species of Verticillium. IV. Pathogenicity of V. albo-atrum and V. dahliae to lucerne and other crops; spread and survival of V. albo-atrum in soil and in weeds; effect upon lucerne production. Annals of Applied Biology 52, 439–451.
| Wilt of lucerne caused by species of Verticillium. IV. Pathogenicity of V. albo-atrum and V. dahliae to lucerne and other crops; spread and survival of V. albo-atrum in soil and in weeds; effect upon lucerne production.Crossref | GoogleScholarGoogle Scholar |
Howell AB, Erwin DC (1995) Characterization and persistence of Verticillium albo-atrum isolated from alfalfa growing in high temperature regions of southern California. Plant Pathology 44, 734–748.
| Characterization and persistence of Verticillium albo-atrum isolated from alfalfa growing in high temperature regions of southern California.Crossref | GoogleScholarGoogle Scholar |
Hu JK, Huang R, Fang R, Shi B, Zhou KH, Chen XJ, Liu YT, Huang RR (2017) A study on artificial inoculation technique for eggplant verticillium wilt at the seedling stage. Acta Agriculturae Universitatis Jiangxiensis 39, 1131–1138.
Inderbitzin P, Bostock RM, Davis RM, Usami T, Platt HW, Subbarao KV (2011) Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium, with the descriptions of five new species. PLoS One 6, e28341
| Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium, with the descriptions of five new species.Crossref | GoogleScholarGoogle Scholar | 22174791PubMed |
Isaac I (1946) Verticillium wilt of sainfoin. Annals of Applied Biology 33, 28–34.
| Verticillium wilt of sainfoin.Crossref | GoogleScholarGoogle Scholar |
Isaac I (1957) Wilt of lucerne caused by species of Verticillium. Annals of Applied Biology 45, 550–558.
| Wilt of lucerne caused by species of Verticillium.Crossref | GoogleScholarGoogle Scholar |
Isaac I, Lloyd ATE (1957) Wilt of lucerne caused by species of Verticillium. Annals of Applied Biology 47, 673–684.
| Wilt of lucerne caused by species of Verticillium.Crossref | GoogleScholarGoogle Scholar |
Jimenez-Diaz RM, Millar RL (1986) Lack of systemic colonization of alfalfa plants after inoculation of uninjured leaves with conidia of Verticillium albo-atrum. Plant Disease 70, 509–515.
| Lack of systemic colonization of alfalfa plants after inoculation of uninjured leaves with conidia of Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Kasson MT, Short DPG, O’Neal ES, Subbarao KV, Davis DD (2014) Comparative pathogenicity, biocontrol efficacy, and multilocus sequence typing of Verticillium nonalfalfae from the invasive Ailanthus altissima and other hosts. Phytopathology 104, 282–292.
| Comparative pathogenicity, biocontrol efficacy, and multilocus sequence typing of Verticillium nonalfalfae from the invasive Ailanthus altissima and other hosts.Crossref | GoogleScholarGoogle Scholar | 24134719PubMed |
Kim JT, Ryu KY, Kim JS, Hahm YI, Yu SH (2003) Verticillium Wilt of Potato Caused by Verticillium albo-atrum in Daegwallyong Area in Korea. The Plant Pathology Journal 19, 184–187.
| Verticillium Wilt of Potato Caused by Verticillium albo-atrum in Daegwallyong Area in Korea.Crossref | GoogleScholarGoogle Scholar |
Leath KT, Pennypacker BW (1990) Verticillium wilt. In ‘Compendium of alfalfa diseases’. (Eds DL Stuteville, DC Erwin) pp. 39–41. (American Phytopathological Society Press: St. Paul, MN, USA)
Li N, Wang W, Bitas V, Subbarao K, Liu X, Kang S (2018) Volatile compounds emitted by diverse Verticillium species enhance plant growth by manipulating auxin signaling. Molecular Plant-Microbe Interactions 31, 1021–1031.
| Volatile compounds emitted by diverse Verticillium species enhance plant growth by manipulating auxin signaling.Crossref | GoogleScholarGoogle Scholar | 29741467PubMed |
Mahuku GS, Platt HW (2002) Molecular evidence that Verticillium albo-atrum Grp 2 isolates are distinct from V. albo-atrum Grp 1 and V. tricorpus. Molecular Plant Pathology 3, 71–79.
| Molecular evidence that Verticillium albo-atrum Grp 2 isolates are distinct from V. albo-atrum Grp 1 and V. tricorpus.Crossref | GoogleScholarGoogle Scholar | 20569311PubMed |
Mamluk OF (1974) A first report on Verticillium wilt of cotton in Iraq. The Plant Disease Reporter 130, 1505–1512.
Mead HW (1955) The effect of fungicides on seedling diseases of legumes and grasses in Saskatchewan. Canadian Journal of Agricultural Science 35, 329–336.
Page MS, Gray FA, Legg DE, Kearl WG (1992) Economic impact and management of Verticillium wilt on irrigated alfalfa hay production in Wyoming. Plant Disease 76, 504–508.
| Economic impact and management of Verticillium wilt on irrigated alfalfa hay production in Wyoming.Crossref | GoogleScholarGoogle Scholar |
Panton CA (1965) The breeding of lucerne, Medicago sativa for resistance to Verticillium albo-atrum. Acta Agriculturae Scandinavica 15, 85–100.
| The breeding of lucerne, Medicago sativa for resistance to Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Pennypacker BW, Leath KT (1983) Dispersal of Verticillium albo-atrum in the xylem of alfalfa. Plant Disease 67, 1226–1229.
| Dispersal of Verticillium albo-atrum in the xylem of alfalfa.Crossref | GoogleScholarGoogle Scholar |
Pennypacker BW, Leath KT, Hill RR (1985) Resistant alfalfa plants as symptomless carriers of Verticillium albo-atrum. Plant Disease 69, 510–511.
| Resistant alfalfa plants as symptomless carriers of Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Resende MLV, Flood J, Cooper RM (1995) Effect of method of inoculation, inoculum density and seedling age at inoculation on the expression of resistance of cocoa (Theobroma cacao) to Verticillium dahliae. Plant Pathology 44, 374–383.
| Effect of method of inoculation, inoculum density and seedling age at inoculation on the expression of resistance of cocoa (Theobroma cacao) to Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |
Robb J, Moukhamedov R, Hu X, Platt H, Nazar RN (1993) Putative subgroups of Verticillium albo-atrum distinguishable by PCR-based assays. Physiological and Molecular Plant Pathology 43, 423–436.
| Putative subgroups of Verticillium albo-atrum distinguishable by PCR-based assays.Crossref | GoogleScholarGoogle Scholar |
Selman IW, Buckley WR (1959) Factors affecting the invasion of tomato roots by Verticillium albo-atrum. Transactions of the British Mycological Society 42, 227–234.
| Factors affecting the invasion of tomato roots by Verticillium albo-atrum.Crossref | GoogleScholarGoogle Scholar |
Sewell GWF, Wilson JF (1964) Occurrence and dispersal of Verticillium conidia in xylem sap of the hop (Humulus lupulus). Nature 204, 901
| Occurrence and dispersal of Verticillium conidia in xylem sap of the hop (Humulus lupulus).Crossref | GoogleScholarGoogle Scholar |
Smith EG, Acharya SN, Huang HC (1995) Economics of growing Verticillium wilt resistant and adapted alfalfa cultivars in Western Canada. Agronomy Journal 87, 1206–1210.
| Economics of growing Verticillium wilt resistant and adapted alfalfa cultivars in Western Canada.Crossref | GoogleScholarGoogle Scholar |
Sumino A, Abe H (1999) Verticillium wilt of sunflower caused by Verticillium dahliae. Annals of the Phytopathological Society of Japan 65, 498–500.
| Verticillium wilt of sunflower caused by Verticillium dahliae.Crossref | GoogleScholarGoogle Scholar |
Trapero C, Díez CM, Rallo L, Barranco D, López-Escudero FJ (2013) Effective inoculation methods to screen for resistance to Verticillium Wilt in olive. Scientia Horticulturae 162, 252–259.
| Effective inoculation methods to screen for resistance to Verticillium Wilt in olive.Crossref | GoogleScholarGoogle Scholar |
Xu S, Li YZ, Nan ZB (2016) First report of Verticillium wilt of alfalfa caused by Verticillium alfalfae in China. Plant Disease 100, 220
| First report of Verticillium wilt of alfalfa caused by Verticillium alfalfae in China.Crossref | GoogleScholarGoogle Scholar |
Xu S, Christensen M, Creamer R, Li YZ (2019) Identification, characterization, pathogenicity and distribution of Verticillium alfalfae in alfalfa plants in China. Plant Disease 103, 1565–1576.
| Identification, characterization, pathogenicity and distribution of Verticillium alfalfae in alfalfa plants in China.Crossref | GoogleScholarGoogle Scholar | 31033401PubMed |
Yorston JM (1983) What is Verticillium wilt? In ‘Verticillium wilt of alfalfa’. (Eds HC Huang, TC Atkinson) pp. 6–12. (Research Branch, Agriculture Canada: Ottawa)
Yu KF, Christie BR, Pauls KP (1993) A comparison of screening techniques for resistance to Verticillium Wilt in alfalfa (Medicago sativa). Journal of Phytopathology 139, 26–32.
| A comparison of screening techniques for resistance to Verticillium Wilt in alfalfa (Medicago sativa).Crossref | GoogleScholarGoogle Scholar |
Zhang QX (1986) New progress in the study of verticillium wilt in Jiangsu province. Agricultural Science Bulletin 5, 21
