<i>Rhizoctonia solani</i> AG-3PT is the major pathogen associated with potato stem canker and black scurf in Jordan

Ziad Jaradat; Hussen Aldakil; Maher Tadros; Mohammad Alboom; Batool Khataybeh; Ziad Jaradat; Hussen Aldakil; Maher Tadros; Mohammad Alboom; Batool Khataybeh

doi:10.3934/agrfood.2023006

AIMS Agriculture and Food

2023, Volume 8, Issue 1: 119-136. doi: 10.3934/agrfood.2023006

Previous Article Next Article

Research article Topical Sections

Rhizoctonia solani AG-3PT is the major pathogen associated with potato stem canker and black scurf in Jordan

1.
Department of Biotechnology and Genetic Engineering, Jordan University of Science and Technology, P. O Box, 3030, Irbid, Jordan
2.
Department of Plant Production, Jordan University of Science and Technology, P. O Box, 3030, Irbid, Jordan
3.
Department of Natural Resources and Environment, Jordan University of Science and Technology, P. O Box, 3030, Irbid, Jordan
4.
Department of Nutrition and Food Technology, Jordan University of Science and Technology, P. O Box, 3030, Irbid, Jordan

Received: 22 August 2022 Revised: 27 November 2022 Accepted: 08 December 2022 Published: 26 December 2022

Rhizoctonia solani (teleomorph: Thanatephorus cucumeris) is a global soil-borne pathogen that severely harms potato crops, leading to significant product losses. Black scurf and stem canker are two manifestations caused by this pathogen, with variable intensity based on the distinctive anastomosis group endemic to the region. During the growing season of 2017 (March and April), 57 different fungus isolates were collected from potato crops farmed in the Jordan Valley. The identity of all the isolates was confirmed by sequencing the internal transcribed spacer (ITS) of the ribosomal DNA gene, and the hyphal interactions were also performed with R. solani isolates. The sequences were deposited in GenBank, where accession numbers were obtained. 21 of the isolates were AG-3PT R. solani, with 98–99% identity to reference strains. Somatic compatibility was determined by hyphal interactions, which showed pairing compatibility among the isolates. Around 86.7% of the pairings were somatically incompatible, indicating a high level of genetic diversity among the isolates, while only 13.3% of the pairings were somatically compatible. Testing for pathogenicity revealed that AG-3PT affected the stems of solanaceous plants, including potatoes, and the roots of other plant species. Based on the findings of this study, R. solani AG-3PT was the primary pathogen associated with potato stem canker and black scurf diseases in Jordan. To our knowledge, this is the first report on this pathogen's isolation and identification in Jordan.
- black scurf,
- pathogenicity,
- Rhizoctonia solani,
- stem canker,
- Thanatephorus cucumeris
Citation: Ziad Jaradat, Hussen Aldakil, Maher Tadros, Mohammad Alboom, Batool Khataybeh. Rhizoctonia solani AG-3PT is the major pathogen associated with potato stem canker and black scurf in Jordan[J]. AIMS Agriculture and Food, 2023, 8(1): 119-136. doi: 10.3934/agrfood.2023006

Related Papers:

Abstract

Rhizoctonia solani (teleomorph: Thanatephorus cucumeris) is a global soil-borne pathogen that severely harms potato crops, leading to significant product losses. Black scurf and stem canker are two manifestations caused by this pathogen, with variable intensity based on the distinctive anastomosis group endemic to the region. During the growing season of 2017 (March and April), 57 different fungus isolates were collected from potato crops farmed in the Jordan Valley. The identity of all the isolates was confirmed by sequencing the internal transcribed spacer (ITS) of the ribosomal DNA gene, and the hyphal interactions were also performed with R. solani isolates. The sequences were deposited in GenBank, where accession numbers were obtained. 21 of the isolates were AG-3PT R. solani, with 98–99% identity to reference strains. Somatic compatibility was determined by hyphal interactions, which showed pairing compatibility among the isolates. Around 86.7% of the pairings were somatically incompatible, indicating a high level of genetic diversity among the isolates, while only 13.3% of the pairings were somatically compatible. Testing for pathogenicity revealed that AG-3PT affected the stems of solanaceous plants, including potatoes, and the roots of other plant species. Based on the findings of this study, R. solani AG-3PT was the primary pathogen associated with potato stem canker and black scurf diseases in Jordan. To our knowledge, this is the first report on this pathogen's isolation and identification in Jordan.

References

[1]	Wibberg D, Genzel F, Verwaaijen B, et al. (2017) Draft genome sequence of the potato pathogen Rhizoctonia solani AG3-PT isolate Ben3. Arch Microbiol 199: 1065–1068. https://doi.org/10.1007/s00203-017-1394-x doi: 10.1007/s00203-017-1394-x
[2]	Boruah S, Dutta P (2021) Fungus mediated biogenic synthesis and characterization of chitosan nanoparticles and its combine effect with Trichoderma asperellum against Fusarium oxysporum, Sclerotium rolfsii and Rhizoctonia solani. Indian Phytopathol 74: 81–93. https://doi.org/10.1007/s42360-020-00289-w doi: 10.1007/s42360-020-00289-w
[3]	Muzhinji N, Truter M, Woodhall JW, et al. (2015) Anastomosis groups and pathogenicity of Rhizoctonia solani and binucleate Rhizoctonia from potato in South Africa. Plant Dis 99: 1790–1802. https://doi.org/10.1094/PDIS-02-15-0236-RE doi: 10.1094/PDIS-02-15-0236-RE
[4]	Rafiq M, Javaid A, Shoaib A (2021) Antifungal activity of methanolic leaf extract of Carthamus oxycantha against Rhizoctonia solani. Pak J Bot 53: 1133–1139. https://doi.org/10.30848/PJB2021-3(17) doi: 10.30848/PJB2021-3(17)
[5]	Brierley JL, Hilton AJ, Wale SJ, et al. (2016) The relative importance of seed-and soil-borne inoculum of Rhizoctonia solani AG-3 in causing black scurf on potato. Potato Res 59: 181–193. https://doi.org/10.1007/s11540-016-9320-1 doi: 10.1007/s11540-016-9320-1
[6]	Muzhinji N, Woodhall JW, Truter M, et al. (2014) Elephant hide and growth cracking on potato tubers caused by Rhizoctonia solani AG3-PT in South Africa. Plant Dis 98: 570–570. https://doi.org/10.1094/PDIS-08-13-0815-PDN doi: 10.1094/PDIS-08-13-0815-PDN
[7]	Larkin RP (2016) Impacts of biocontrol products on Rhizoctonia disease of potato and soil microbial communities, and their persistence in soil. Crop Prot 90: 96–105. https://doi.org/10.1016/j.cropro.2016.08.012 doi: 10.1016/j.cropro.2016.08.012
[8]	Stefańczyk E, Sobkowiak S, Brylińska M, et al. (2016) Diversity of Fusarium spp. associated with dry rot of potato tubers in Poland. Eur J Plant Pathol 145: 871–884. https://doi.org/10.1007/s10658-016-0875-0 doi: 10.1007/s10658-016-0875-0
[9]	Mengesha WK, Gill WM, Powell SM, et al. (2017) A study of selected factors affecting efficacy of compost tea against several fungal pathogens of potato. J Appl Microbiol 123: 732–747. https://doi.org/10.1111/jam.13530 doi: 10.1111/jam.13530
[10]	Banville GJ (1989) Yield losses and damage to potato plants caused by Rhizoctonia solani Kuhn. Am Potato J 66: 821–834. https://doi.org/10.1007/BF02853963 doi: 10.1007/BF02853963
[11]	Zhang J, Wang Y, Zhao Y, et al. (2020) Transcriptome analysis reveals Nitrogen deficiency induced alterations in leaf and root of three cultivars of potato (Solanum tuberosum L.). PloS One 15: e0240662. https://doi.org/10.1371/journal.pone.0240662 doi: 10.1371/journal.pone.0240662
[12]	Abu‐El Samen FM, Al‐Bdour NM (2011) Prevalence of fungal and fungus‐like diseases on potato seed tubers imported from Europe to Jordan. EPPO Bull 41: 445–452. https://doi.org/10.1111/j.1365-2338.2011.02514.x doi: 10.1111/j.1365-2338.2011.02514.x
[13]	Carling DE, Kuninaga S, Brainard KA (2002) Hyphal anastomosis reactions, rDNA-internal transcribed spacer sequences, and virulence levels among subsets of Rhizoctonia solani anastomosis group-2 (AG-2) and AG-BI. Phytopathology 92: 43–50. https://doi.org/10.1094/PHYTO.2002.92.1.43 doi: 10.1094/PHYTO.2002.92.1.43
[14]	Woodhall JW, Lees AK, Edwards SG, et al. (2007) Characterization of Rhizoctonia solani from potato in Great Britain. Plant Pathol 56: 286–295. https://doi.org/10.1111/j.1365-3059.2006.01545.x doi: 10.1111/j.1365-3059.2006.01545.x
[15]	Inokuti EM, Reis A, Ceresini PC, et al. (2019) Diversity and pathogenicity of anastomosis groups of Rhizoctonia associated with potato stem canker and black scurf diseases in Brazil. Eur J Plant Pathol 153: 1333–1339. https://doi.org/10.1007/s10658-018-01627-5 doi: 10.1007/s10658-018-01627-5
[16]	Carling DE, Leiner RH (1990) Virulence of isolates of Rhizoctonia solani AG-3 collected from potato plant organs and soil. Plant Dis 74: 901–3. https://doi.org/10.1094/PD-74-0901 doi: 10.1094/PD-74-0901
[17]	Liu D, Coloe S, Baird R, et al. (2000) Rapid mini-preparation of fungal DNA for PCR. J Clin Microbiol 38: 471–471. https://doi.org/10.1128/JCM.38.1.471-471.2000 doi: 10.1128/JCM.38.1.471-471.2000
[18]	Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes‐application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x doi: 10.1111/j.1365-294X.1993.tb00005.x
[19]	WhiteTJ, Bruns T, Lee SJ, et al. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc: Guide Methods Appl 18: 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1 doi: 10.1016/B978-0-12-372180-8.50042-1
[20]	Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+ C-content biases. Mol Biol Evol 9: 678–687.
[21]	Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
[22]	Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x doi: 10.1111/j.1558-5646.1985.tb00420.x
[23]	Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci 101: 11030–11035. https://doi.org/10.1073/pnas.0404206101 doi: 10.1073/pnas.0404206101
[24]	Kumar S, Stecher G, Li M, et al. (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35: 1547. https://doi.org/10.1093/molbev/msy096 doi: 10.1093/molbev/msy096
[25]	Bandoni RJ (1979) Safranin O as a rapid nuclear stain for fungi. Mycologia 71: 873–874. https://doi.org/10.1080/00275514.1979.12021088 doi: 10.1080/00275514.1979.12021088
[26]	Carling DE (1996) Grouping in Rhizoctonia solani by hyphal anastomosis reaction. In: Rhizoctonia species: taxonomy, molecular biology, ecology, pathology and disease control Springer, Dordrecht, 37–47. https://doi.org/10.1007/978-94-017-2901-7_3
[27]	MacNish GC, Carling DE, Brainard KA (1997) Relationship of microscopic and macroscopic vegetative reactions in Rhizoctonia solani and the occurrence of vegetatively compatible populations (VCPs) in AG-8. Mycol Res 101: 61–68. https://doi.org/10.1017/S0953756296002171 doi: 10.1017/S0953756296002171
[28]	Carling DE, Leiner RH (1986) Isolation and characterization of Rhizoctonia solani and binucleata R. solani-like fungi from aerial stems and subterranean organs of potato plants. Phytopathology 76: 725–729. https://doi.org/10.1094/Phyto-76-725 doi: 10.1094/Phyto-76-725
[29]	Classic Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x doi: 10.1111/j.1399-3054.1962.tb08052.x
[30]	Yang S, Min F, Wang W, et al. (2017) Anastomosis group and pathogenicity of Rhizoctonia solani associated with stem canker and black scurf of potato in Heilongjiang Province of China. Am J Potato Res 94: 95–104. https://doi.org/10.1007/s12230-016-9535-3 doi: 10.1007/s12230-016-9535-3
[31]	Ibrahim ME (2017) In vitro antagonistic activity of Trichoderma harzianum against Rhizoctonia solani the causative agent of potato black scurf and stem canker. Egypt J Bot 57: 173–185. https://doi.org/10.21608/ejbo.2017.903.1067 doi: 10.21608/ejbo.2017.903.1067
[32]	Anguiz R, Martin C (1989) Anastomosis groups, pathogenicity and other characteristics of Rhizoctonia solani isolated from potato in Peru. Plant Dis 73: 99–201. https://doi.org/10.1094/PD-73-0199 doi: 10.1094/PD-73-0199
[33]	Balali GR, Neate SM, Scott ES, et al. (1995) Anastomosis group and pathogenicity of isolates of Rhizoctonia solani from potato crops in South Australia. Plant Pathol 44: 1050–1057. https://doi.org/10.1111/j.1365-3059.1995.tb02664.x doi: 10.1111/j.1365-3059.1995.tb02664.x
[34]	Campion C, Chatot C, Perraton B, et al (2003) Anastomosis groups, pathogenicity and sensitivity to fungicides of Rhizoctonia solani isolates collected on potato crops in France. Eur J Plant Pathol 109: 983–992. https://doi.org/10.1023/B:EJPP.0000003829.83671.8f doi: 10.1023/B:EJPP.0000003829.83671.8f
[35]	Truter M, Wehner FC (2004) Anastomosis grouping of Rhizoctonia solani associated with black scurf and stem canker of potato in South Africa. Plant Dis 88: 83–83. https://doi.org/10.1094/PDIS.2004.88.1.83B doi: 10.1094/PDIS.2004.88.1.83B
[36]	Fiers M, Edel-Hermann V, Héraud C, et al. (2011) Genetic diversity of Rhizoctonia solani associated with potato tubers in France. Mycologia 103: 1230–1244. https://doi.org/10.3852/10-231 doi: 10.3852/10-231
[37]	Das S, Shah FA, Butler RC, et al. (2014) Genetic variability and pathogenicity of R hizoctonia solani associated with black scurf of potato in New Zealand. Plant Pathol 63: 651–666. https://doi.org/10.1111/ppa.12139 doi: 10.1111/ppa.12139
[38]	Lehtonen MJ, Somervuo P, Valkonen JP (2008) Infection with Rhizoctonia solani induces defense genes and systemic resistance in potato sprouts grown without light. Phytopathology 98: 1190–1198. https://doi.org/10.1094/PHYTO-98-11-1190 doi: 10.1094/PHYTO-98-11-1190
[39]	Misawa T, Kuninaga S (2010) The first report of tomato foot rot caused by Rhizoctonia solani AG-3 PT and AG-2-Nt and its host range and molecular characterization. J Gen Plant Pathol 76: 310–319. https://doi.org/10.1007/s10327-010-0261-2 doi: 10.1007/s10327-010-0261-2
[40]	Gonzalez M, Pujol M, Metraux JP, et al. (2011) Tobacco leaf spot and root rot caused by Rhizoctonia solani Kühn. Mol Plant Pathol 12: 209–216. https://doi.org/10.1111/j.1364-3703.2010.00664.x doi: 10.1111/j.1364-3703.2010.00664.x
[41]	Ceresini PC, Shew HD, Vilgalys RJ, et al. (2002) Genetic diversity of Rhizoctonia solani AG-3 from potato and tobacco in North Carolina. Mycologia 94: 437–449. doi: 10.1080/15572536.2003.11833209
[42]	Campos APD, Ceresini PC (2006) Somatic incompatibility in Rhizoctonia solani AG-1 IA of soybean. Summa Phytopathol 32: 247–254. doi: 10.1590/S0100-54052006000300006
[43]	Anderson NA (1982) The genetics and pathology of Rhizoctonia solani. Annu Rev Phytopathol 20: 329–347. doi: 10.1146/annurev.py.20.090182.001553
[44]	Sneh B, Jabaji-Hare S, Neate SM, et al. (2013) Rhizoctonia species: Taxonomy, molecular biology, ecology, pathology and disease control. Springer Science & Business Media.
[45]	Nelson B, Helms T, Christianson T, et al. (1996) Characterization and pathogenicity of Rhizoctonia from soybean. Plant Dis 80: 74–80. doi: 10.1094/PD-80-0074
[46]	Tewoldemedhin YT, Lamprecht SC, McLeod AD, et al. (2006) Characterization of Rhizoctonia spp. recovered from crop plants used in rotational cropping systems in the Western Cape province of South Africa. Plant Dis 90: 1399–1406. doi: 10.1094/PD-90-1399

Reader Comments

Your name:*

Email:*
© 2023 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)