Bacterial Species as Causative Agents Involved in Pistachios Dieback in Iran

Subject Areas : Plant Pathology

Elham Tavasoli ¹ , Mohammad Moradi ² , Nader Hasanzadeh ³ , Pejman Khodaygan ⁴ , Claudia Probst ⁵

1 - Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran, Iran
2 - Pistachio Research Center, Horticultural Science Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Rafsanjan, Iran
3 - Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran, Iran
4 - Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University, Rafsanjan, Iran
5 - Agriculture Technology and management Department, University of Applied Sciences Upper Austria, School of Engineering, Wels, Austria

Received: 2023-07-25 Accepted : 2024-01-28 Published : 2024-02-04

Keywords: pathogenicity, Pistacia vera, Bacterial pathogens, Crop damage,

Abstract :

Pistachio dieback (DBP) is a significant disease affecting pistachio trees in Iran, and it has emerged as a serious problem in Kerman province in recent years. This study investigates the role of bacteria as causal agents of DBP under laboratory and field conditions. Samples were collected from infected pistachio orchards in Kerman province from 2015 to 2016. The ability of bacterial isolates to induce disease and colonize vascular tissues was studied using various inoculation methods. Identification of isolates was carried out using biochemical and physiological assays, amplification of the 16S rDNA region, and partial analyses of the gyrA gene. A total of 281 bacterial isolates were obtained from infected trees, of which 148 induced a hypersensitivity reaction on tobacco leaves. Among these, 128 isolates were able to colonize vascular tissues in sub-bark inoculations of pistachio branches under laboratory conditions. In field experiments, 24 selected isolates were able to spread in vascular tissues of pistachio branches and twigs using sub-bark and apical inoculation methods, although disease severity varied. Staphylococcus pasteuri, Bacillus pumilus, Bacillus sp., Acinetobacter radioresistens, Xanthomonas sp., Curtobacterium flaccumfaciens, Pseudarthrobacter oxydans, and Pseudomonas koreensis were identified as being involved in the dieback of pistachio trees. This work demonstrates that a wide range of bacterial genera and species may be involved in DBP, and urgent strategies should be considered for managing the disease.

References:

Alizadeh A, Alaei H, Ershad D (2000) Etiological study on dieback disease of pistachio trees in Rafsanjan. Journal of Modares Agricultural Sciences. 1(2), 53-63.
Agrios GN (2005) Plant Pathology. 5th Ed. Elsevier Academic Press, Amsterdam. pp. 952.
Aminaee MM, Ershad D (1987) Die-back of young shoots of pistachio trees in Kerman province. In: Proceeding of 11th Iranian Plant Protection Congress: 216.
Araújo WL, Marcon J, Maccheroni Jr W, Van Elsas JD, Van Vuurde JW, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Applied and Environmental Microbiology. 68(10), 4906-4914.
Ash C, Farrow JA, Dorsch M, Stackebrandt E, Collins MD (1991) Comparative analysis of Bacillus anthracis, Bacillus cereus, and related species on the basis of reverse transcriptase sequencing of 16S rRNA. International Journal of Systematic and Evolutionary Microbiology. 41(3), 343-346.
Bacon CW, Hinton DM (2006) Bacterial endophytes: The endophytic niche, its occupants, and its utility. In: Gnanamanickam SS (Ed) Plant-Associated Bacteria. 155–194.
Baldan E, Nigris S, Populin F, Zottini M, Squartini A, Baldan B (2014) Identification of culturable bacterial endophyte community isolated from tissues of Vitis vinifera “Glera”. Plant Biosystems-An International Journal Dealing with all Aspects of Plant Biology. 148(3), 508-516.
Baradaran GR, Ghasemi A (2010) Introducing Bacillus licheniformis as the causal agent of pistachio dieback in Iran. Archives of Phytopathology and Plant Protection. 43(6), 597-601.
Behzadi Rad P, Roozban MR, Karimi S, Ghahremani R, Vahdati K (2021) Osmolyte accumulation and sodium compartmentation has a key role in salinity tolerance of pistachios rootstocks. Agriculture. 11(8), 708.
Bell CR, Dickie GA, Harvey WLG, Chan JWYF (1995) Endophytic bacteria in grapevine. Canadian Journal of Microbiology. 41(1), 46-53.
Bulgari D, Casati P, Quaglino F, Bianco PA (2014) Endophytic bacterial community of grapevine leaves influenced by sampling date and phytoplasma infection process. BMC Microbiology. 14(1), 1-11.
Chun J, Bae KS (2000) Phylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA gene sequences. Antonie van Leeuwenhoek. 78(2), 123-127.
Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology. 71(9), 4951-4959.
Derviş S, Türkölmez Ş, Çiftçi O, Ulubaş Serçe Ç, Dikilitas M (2019) First Report of Neoscytalidium dimidiatum Causing Canker, Shoot Blight, and Root Rot of Pistachio in Turkey. Plant Disease. 103(6),1411-1411.
Di Fiore S, Del Gallo M (1995) Endophytic bacteria: their possible role in the host plant. In: Fendrik I, del Gallo M, Vanderleyden J, de Zamaroczy M (Eds) Azospirillum VI and Related Microorganisms. NATO ASI Series, Volume 37. Springer, Berlin, Heidelberg. 169-187.
Drancourt M, Raoult D (2002) rpoB gene sequence-based identification of Staphylococcus species. Journal of Clinical Microbiology. 40(4),1333-1338.
Dunleavy JM (1989) Curtobacterium plantarum sp. nov. is ubiquitous in plant leaves and is seed transmitted in soybean and corn. International Journal of Systematic and Evolutionary Microbiology. 39(3), 240-249.
Edwards M, Taylor C (1998) Pistachio canker: the story so far. In: Proceedings of the Eighth Australian Nut Industry Council Conference. Victoria, Australia: Australian Nut Industry Council. 31-32.
Eslami M, Nasibi F, Manouchehri Kalantari K, Khezri M, Oloumi H (2019) Effect of exogenous application of l-arginine and sodium nitroprusside on fruit abscission and physiological disorders of pistachio (Pistacia Vera L.) Scions. International Journal of Horticultural Science and Technology. 6(1), 51-62.
Facelli E, Taylor C, Scott E, Emmett R, Fegan M, Sedgley M (2002) Bacterial dieback of pistachio in Australia. Australasian Plant Pathology. 31(1), 95.
Facelli E, Taylor C, Scott E, Fegan M, Huys G, Noble RD, Swings J, Sedgley M (2005) Identification of the causal agent of pistachio dieback in Australia. European Journal of Plant Pathology. 112(2), 155-165.
Facelli E, Taylor C, Williams NM, Emmett RW, Sedgley M, Joyce CK, Scott ES (2009) Location of Xanthomonas translucens in pistachio trees. Australasian Plant Pathology. 38(6), 584-593.
García-Martínez J, Bescós I, Rodríguez-Sala JJ, Rodríguez-Valera F (2001) RISSC: a novel database for ribosomal 16S–23S RNA genes spacer regions. Nucleic Acids Research. 29(1), 178-180.
Ghelichi M, Mohammadi A, Haghdel M, Eskandari A (2012) Distribution of pistachio die-back in Khorasan-Razavi province and application of some fungicides for the disease control. Journal of Nuts. 3(1), 23-28.
Giblot-Ducray D, Marefat A, Gillings MR, Parkinson NM, Bowman JP, Ophel-Keller K, Taylor C, Facelli E, Scott ES (2009) Proposal of Xanthomonas translucens pv. pistaciae pv. nov., pathogenic to pistachio (Pistacia vera). Systematic and Applied Microbiology. 32(8), 549-557.
Heidarian R, Fotouhifar KB, Debets AJ, Aanen DK (2018) Phylogeny of Paecilomyces, the causal agent of pistachio and some other trees dieback disease in Iran. PLoS One. 13(7), e0200794.
Hosseini N, Rezanejad F, ZamaniBahramabadi E (2022) Effects of soil texture, irrigation intervals, and cultivar on some nut qualities and different types of fruit blankness in pistachio (Pistacia vera L.). International Journal of Horticultural Science and Technology. 9(1), 41-53.
Jackson RW (2009) Plant pathogenic bacteria: genomics and molecular biology, Caister Academic Press
Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annual Reviews of Plant Biology. 58, 435-458.
Joung KB, Côté JC (2002) Evaluation of ribosomal RNA gene restriction patterns for the classification of Bacillus species and related genera. Journal of Applied Microbiology. 92(1), 97-108.
Jukes TH, Cantor CR (1969). Evolution of protein molecules. Mammalian Protein Metabolism. 3, 21-132.
Kazerooni EA, Maharachchikumbura SS, Adhikari A, Al-Sadi AM, Kang SM, Kim LR, Lee IJ (2021) Rhizospheric Bacillus amyloliquefaciens protects Capsicum annuum cv. Geumsugangsan from multiple abiotic stresses via multifarious plant growth-promoting attributes. Frontiers in Plant Science. 12, 821.
Klement Z, Rudolph K, Sands DC (1990) Methods in phytobacteriology. Akademiai Kiado, Budapest. pp. 568.
Khan IA, Khan A, Asif H, Jiskani MM, Mühlbach HP, Azim MK (2014) Isolation and 16S rDNA sequence analysis of bacteria from dieback affected mango orchards in southern Pakistan. Pakistan Journal of Botany. 46(4),1431-1435.
Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF (Eds) Microbial Endophytes, Marcel Dekker, New York. 199-233.
Kurt Ş, Uysal A, Soylu EM, Kara M, Soylu S (2019) First record of Neoscytalidium novaehollandiae associated with pistachio dieback in the southeastern Anatolia region of Turkey. Mycologia Iranica. 6(1), 55-57.
Lelliott RA, Stead DE (1987) Methods for the diagnosis of bacterial diseases of plants. Blackwell Scientific Publications. pp. 215.
Li C, Junttila O, Palva ET (2004) Environmental regulation and physiological basis of freezing tolerance in woody plants. Acta Physiologiae Plantarum. 26(2), 213-222.
Lodewyckx C, Vangronsveld J, Porteous F, Moore ER, Taghavi S, Mezgeay M, der Lelie DV (2002) Endophytic bacteria and their potential applications. Critical Reviews in Plant Sciences. 21(6), 583-606.
Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Applied and Environmental Microbiology. 64(2),795-799.
Marefat A, Scott ES, Ophel‐Keller K, Sedgley M (2006) Genetic, phenotypic and pathogenic diversity among Xanthomonads isolated from pistachio (Pistacia vera) in Australia. Plant Pathology. 55(5), 639-649.
Marefat A, Ophel-Keller K, Scott ES, Sedgley M (2006) The use of ARMS PCR in detection and identification of Xanthomonads associated with pistachio dieback in Australia. European Journal of Plant Pathology. 116(1), 57-68.
McClean AE, Kluepfel DA (2010) Biology of Brenneria rubrifaciens: screening for genes involved in pathogenesis. línea http://cekings. ucdavis. edu/files/47896. pdf.
Michailides TJ, Ogawa JM (1985) Sources of inoculum, epidemiology and control of Botryosphaeria shoot and panicle blight of pistachio. Californai Pistachio Industry. Annual Report, Crop Year. 86, 87-91.
Miché L, Battistoni F, Gemmer S, Belghazi M, Reinhold-Hurek B (2006) Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Molecular Plant-Microbe Interactions. 19(5), 502-511.
Misaghi IJ, Donndelinger CR (1990) Endophytic bacteria in symptom-free cotton plants. Phytopathology. 80(9), 808-811.
Mocali S, Bertelli E, Di Cello F, Mengoni A, Sfalanga A, Viliani F, Caciotti A, Tegli S, Surico G, Fani R (2003) Fluctuation of bacteria isolated from elm tissues during different seasons and from different plant organs. Research in Microbiology. 154(2), 105-114.
Mohammadi AH, Haghdel M, Moghaddam MM, Banihashemi Z (2006) Current status of Verticillium wilt disease of pistachio trees in Iran. Acta Horticulturae. 726, 631-636.
Nazoori F, ZamaniBahramabadi E, Mirdehghan H (2022) Effect of sulfur pesticide on the quality of fresh pistachios in cold storage. International Journal of Horticultural Science and Technology. 9(4), 453-462.
Nazoori F, ZamaniBahramabadi E, Mirdehghan H, Yousefi M (2022) Preharvest application of sulfur as pesticide on fresh hull and kernel of pistachio (Pistacia vera L.). International Journal of Horticultural Science and Technology. 9(1), 117-129.
Nishimura Y, Ino T, Iizuka H (1988) Acinetobacter radioresistens sp. nov. isolated from cotton and soil. International Journal of Systematic and Evolutionary Microbiology. 38(2), 209-211.
Ocho FL (2006) Biochemical, pathological and genetic characterization of strains of Ralstonia solanacearum (Smith) from Ethiopia and biocontrol of R. solanacearum with bacterial antagonists (Doctoral dissertation, Hannover, Univ., Diss., 2006).
Palmisano MM, Nakamura LK, Duncan KE, Istock CA, Cohan FM (2001) Bacillus sonorensis sp. nov., a close relative of Bacillus licheniformis, isolated from soil in the Sonoran Desert, Arizona. International Journal of Systematic and Evolutionary Microbiology. 51(5), 1671-1679.
Renaut J, Hoffmann L, Hausman JF (2005) Biochemical and physiological mechanisms related to cold acclimation and enhanced freezing tolerance in poplar plantlets. Physiologia Plantarum. 125(1), 82-94.
Rooney AP, Price NP, Ehrhardt C, Swezey JL, Bannan JD (2009) Phylogeny and molecular taxonomy of the Bacillus subtilis species complex and description of Bacillus subtilis subsp. inaquosorum subsp. nov. International Journal of Systematic and Evolutionary Microbiology. 59(10), 2429-2436.
Rumbos IC (1986) Isolation and identification of Eutypa lata from Pistacia vera in Greece. Journal of Phytopathology. 116(4), 352-357.
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution. 4, 406-425.
Schaad NW, Jones JB, Chun W (2001) Laboratory guide for the identification of plant pathogenic bacteria (No. Ed. 3). American Phytopathological Society (APS Press). pp. 373.
Shah J (2009) Plants under attack: systemic signals in defense. Current Opinion in Plant Biology. 12(4), 459-464.
Takahashi Y, Takahashi K, Sato M, Watanabe K, Kawano T (1997) Bacterial leaf rot of Odontioda orchids caused by Enterobacter cloacae. Japanese Journal of Phytopathology. 63(3),164-169.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution. 30, 2725-2729.
Tarighi S, Rahimian H (2001) Canker and leaf spot of pistachio caused by Xanthomonas sp. Iranian Journal of Plant Pathology. 37, 161-162.
Ulrich K, Ulrich A, Ewald D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiology Ecology. 63(2), 169-180.
Valdez N, Karlovsky P, Dobrindt L, Hoque MI, Sarker RH, Tantau H, Mühlbach HP (2013) Role of bacteria in dieback disease of Dalbergia sissoo Roxb. Bangladesh. Journal of Botany. 42(1), 1-16.
Vandamme P, Pot B, Gillis M, De Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiological Reviews. 60(2), 407-438.
Vidaver AK (1982) The plant pathogenic Corynebacteria. Annual Reviews in Microbiology. 36(1), 495-517.
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology. 173(2), 697-703.