Document Type : Plant Pathology
Authors
1 , Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran
2 Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran
3 Department of Industrial and Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology, Tehran
4 Researcher, Department of Biodiversity, Boom Zista Institute, Vancouver, British Columbia, Canada
5 Assistant Professor, Department of Plant Breeding and Biotechnology, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran
Abstract
Common bacterial blight disease (CBB) of bean (Phaseolus vulgaris) caused by Xanthomonas phaseoli (Xp) is considered as one of the most deleterious pathogens for bean production in the world. In this study, 105 samples were collected from asymptomatic wild fabaceous plants, i.e. Astragalus ovinus, Vicia villosa and Vicia lutea, grown in Zagros forests of Iran. The plant samples were cultured on nutrient agar and purified. The isolates were then screened for some important criteria for biological control such as phosphate solubilization, protease activity, IAA and H2S production, and antagonistic effect. Three endophytic bacterial isolates were found as potential biocontrol agents against Xp. Based on key biochemical tests and comparative analysis of the partial 16S rDNA sequences, the isolates were identified as Pseudomonas fluorescens and two Bacillus species. Under greenhouse conditions, all the three strains significantly increased shoot and root lengths in bean plants at the 5% level (P < 0.05) and decreased disease severity above 70%. This is the first report on the presence and capabilities of endophytic bacteria from wild leguminous plants in the Zagros Mountain steppe forests of Iran.
Keywords
ABO-ELYOUSR, K. A. and H. H. El-HENDAWY, 2008. Integration of Pseudomonas fluorescens and acibenzolar-S-methyl to control bacterial spot disease of tomato. Crop Protection 27: 1118-1124.
AKHANI, H., M. DJMALI, A. GHORBANALIZADEH and E. RAMEZANI, 2010. Plant biodiversity of Hyrcanian relict forests, N Iran: an overview of the flora, vegetation, palaeoecology and conservation. Pakistan Journal of Botany 42: 231-258.
AKINRINLOLA, R J., G. Y. YUEN, R A. DRIJBER and A.O. ADESEMOYE, 2018. Evaluation of Bacillus Strains for plant growth promotion and predictability of efficacy by in vitro physiological traits, International Journal of Microbiology 2018: 11.
ALSTROM, S. and R.G. BURNS, 1989. Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biology and Fertility of Soils 7: 232-238.
ALTSCHULl, S.F., T.L. MADDEN and A.A. SCHAFFER, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
AQUINO-MARTINEZ, J.G., L.M. VAZQUEZ-GARCIA and B.G. REYES-REYES, 2008. Biocontrol in vitro e in vivo de Fusarium oxysporum Schlecht. f. sp. dianthi (Prill. Y Delacr.) snyder y Hans. Con hongos antagonistas nativos de la zona florícola de Villa Guerrero. Revista Mexicana de Fitopatolgia 26:127-113.
ARSHADI, N., E. SEDAGHATFAR, A.GOLNARAGHI and T. GLARE, 2019. Endophytic characteristic of entomopathogenic fungi Beauveria on bean plant. Bioagrica 1:1-9.
BASHIR, S., A. IQBAL and S. HASNAIN, 2019. Comparative analysis of endophytic bacterial diversity between two varieties of sunflower Helianthus annuus with their PGP evaluation. Saudi Journal of Biological Sciences 27:720-726.
BENEDUZI, A., A. AMBROSINI and L.M. PASSAGLIA, 2012. Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genetics and Molecular Biology 4:1044-1051.
BYRNE, J., A. DIANESE, H. CAMPBELL, D. CUPPEL, F. LOUWS and M. WILSON, 2005. Biological control of bacterial spot of tomato under field conditions at several locations in North America. Biological Control 32: 408-418.
CHOWDHURY, S.P., A. HARTMANN, X. GAO and R. Borriss, 2015. Biocontrol mechanism by root associated Bacillus amyloliquefaciens FZB42. Front Microbioly 6:780.
COMPANT, S., B. DUFFY, J. NOWAK, C. CLEMENT and E. BARKA, 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Applied and Environmental Microbiology 71: 4951-4959.
COSTA, L., M. QUEIROZ, A. BORGES, C. MORAES and E. ARAUJO, 2012. Isolation and characterization of endophytic bacteria isolated from the leaves of the common bean (Phaseolus vulgaris). Brazilian Journal of Microbiology 43:1562-1575.
DAUNGFU, O., S. YOUPENSUK and S. LUMYONG, 2019. Endophytic bacteria isolated from Citrus plants for biological Control of citrus canker in lime plants. Tropical Life Sciences Research 30: 73.
DE SOUZA, J., M. DE BOER, P. DE WAARD, T. VAN BEEK and J. RAAIJMAKERS, 2003. Biochemical, genetic, and zoosporicidal properties of cyclic lipopeptide surfactants produced by Pseudomonas fluorescens. Applied and Environmental Microbiology 69:7161-7172.
DHANYA, M. and C. MARY, 2007. Management of bacterial blight of anthurium (Anthurium andreanum Linden.) using ecofriendly materials. Journal of Tropical Agriculture 44: 74-75.
ETESAMI, H., H. HMIRSYEDHOSSEINI and A. ALIKHANI, 2013. Rapid screening of berseem clover (Trifolium alexandrinum) endophytic bacteria for rice plant seedlings growth-promoting agents. Soil Science 9: 9.
ETMINANI, F. and B. HARIGHI, 2018. Isolation and identification of endophytic bacteria with plant growth promoting activity and biocontrol potential from wild pistachio trees. The Plant Pathology Journal 34: 208.
FELSENSTEIN, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
FENG, H., Y. LI., Q. LIU., 2013. Endophytic bacterial communities in tomato plants with differential resistance to Ralstonia solanacearum. African Journal of Microbiology Research 7: 1311-1318.
FREITAS, D. B., M. P. REIS, C. I. LIMA BITTENCOURT, P. S. COSTA, P.S. ASSIS, E. CHARTONE SOUZA and A. M. NASCIMENTO, 2008. Genotypic and phenotypic diversity of Bacillus spp. isolated from steel plant waste. BMC Research Notes 1: 92.
GAMEZ, R., M. CARDINALE, M. MONTES, S. RAMIREZ, S. SCHNELL and F. RODRIGUEZ, 2019. Screening, plant growth promotion and root colonization pattern of two rhizobacteria (Pseudomonas fluorescens Ps006 and Bacillus amyloliquefaciens Bs006) on banana cv. Williams (Musa acuminate Colla). Microbiological Research 220: 12-20.
GHORBANI, S. and B. HARIGHI, 2018. Characterization of endophytic bacteria with plant growth promotion and biological control potential isolated from walnut trees. Forest Pathology 48: 12403.
GOODWIN, P. and C. SOPHER, 1994. Brown pigmentation of Xanthomonas campestris pv. phaseoli associated with homogentisic acid. Canadian Journal of Microbiology 40: 28-34.
GRAHAM, P. and P. RANALLI, 1997. Common bean (Phaseolus vulgaris L.). Field Crops Research 53: 131-146.
GUPTA, M., S. KIRAN, A. GULATI, B. SINGH and R.TEWARI, 2012. Isolation and identification of phosphate solubilizing bacteria able to enhance the growth and aloin-A biosynthesis of Aloe barbadensis Miller. Microbiological Research 167: 358-363.
HALL, T.A., 1999. BioEdit a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
HEIDARI, M., S. ATTAR ROSHAN and K.H. HATAMI, 2010. The evaluation of herb layer biodiversity in relation to physiographical factors in south of Zagros forest ecosystem (Case study: Dalab protected area). Renewable Natural Resources 1:28- 42.
HERRERA, S., C. GROSSI, M. ZAWOZNIK and M. GROPPA, 2016. Wheat seeds harbour bacterial endophytes with potential as plant growth promoters and biocontrol agents of Fusarium graminearum. Microbiological Research 186: 37-43.
JALEEL, C.A., P. MANIVANNAN, B. SANKAR, A. KISHOREKUMAR, R. GOPI, R. SOMASUNDARAM and R. PANNEERSELVAM, 2007. Pseudomonas fluorescens enhances biomass yield and ajmalicine production in Catharanthus roseus under water deficit stress. Colloids and Surfaces B: Biointerfaces 60: 7-11.
KAN, F.L., Z.Y. CHEN, E.T. WANG, C.F. TIAN, X.H. SUI and W.X CHEN, 2007. Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai–Tibet plateau and in other zones of China. Archives of Microbiology 188: 103-115.
KANG, Y., M. SHEN, H. WANG, Q. ZHAO and S. YIN, 2012. Biological control of tomato bacterial wilt caused by Ralstonia solanacearum with Erwinia persicinus RA2 and Bacillus pumilus WP8. Chinese Journal of Biological Control 28: 255-261.
KALAM, S., A. BASU and A.R. PODILE, 2020. Functional and molecular characterization of plant growth promoting Bacillus isolates from tomato rhizosphere. Heliyon 6: 04734.
KEPCZYNSKA, E. and P. KARCZYNSKI, 2020. Medicago truncatula root developmental changes by growth-promoting microbes isolated from Fabaceae, growing on organic farms, involve cell cycle changes and WOX5 gene expression. Planta 251: 25.
KHAYI, S., Y.R. DES ESSARTS, S. MONDY, M. MOUMNI M, V. HELIAS, A. BEURY-CIROU and D. FAURE, 2015. Draft genome sequences of the three Pectobacterium-antagonistic bacteria Pseudomonas brassicacearum PP1-210F and PA1G7 and Bacillus simplex BA2H3. Genome Announc 3: 01497-01414.
KLOEPPER, J., S. TUZUN, L. LIU and G. WEI, 1993. Plant growth-promoting rhizobacteria as inducers of systemic disease resistance. Pest management: biologically based technologies. American Chemical Society Books, Washington DC: 156-165.
KOBAYASHI, D.Y. and J.D. PALUMBO, 2000. Microbial Endophytes. In: Bacon Ch. W, White J. Bacterial endophytes and their effects on plants and uses in agriculture. In Microbial Endophytes 9: 213-250.
KIMURA, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111-120.
KUMAR, S., G. STECHER, M. LI, C H. KNYAZ and K. Tamura, 2018. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution 35:1547–1549.
KRISHNAN, N., GANDHI, K., PEERAN, M. F., KUPPUSAMI, P. and R.THIRUVENGADAM, 2015. Molecular characterization and in vitro evaluation of endophytic bacteria against major pathogens of rice. African Journal of Microbiology Research 9: 800-813.
LARRAN, S., M. SIMON, M. MORENO, M. SIURANA and A. PERELLÓ, 2016. Endophytes from wheat as biocontrol agents against tan spot disease. Biological Control 92: 17-23.
LI, J. H., E.T. WANG, W.F. CHEN and W.X. CHEN, 2008. Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heilongjiang province of China. Soil Biology and Biochemistry 40: 238-246.
LI, H., A. SOARES. M.S. TORRES, M. BERGEN and J.M. WHITE, 2015. Endophytic bacterium, Bacillus amyloliquefaciens, enhances ornamental host resistance to diseases and insect pests, Journal of Plant Interactions, 10: 224-229.
LIU, C., X. CHEN, T. LIU, B. LIAN, Y. GU, V. CAER and B. WANG, 2007. Study of the antifungal activity of Acinetobacter baumannii LCH001 in vitro and identification of its antifungal components. Applied Microbiology and Biotechnology 76: 459-466.
LIU, Y., K. TENG, T. WANG, E. DONG, M. ZHANG, Y. TAO and J. ZHONG, 2020. Antimicrobial Bacillus velezensis HC6: production of three kinds of lipopeptides and biocontrol potential in maize. Journal of Applied Microbiology 128: 242-254.
LIU, K.E., J.A. MCINROY, C.H. HU and J.W. KLOEPPER, 2018. Mixtures of plant-growth-promoting rhizobacteria enhance biological control of multiple plant diseases and plant-growth promotion in the presence of pathogens. Plant Disease 102:68-72.
LODEWYCKX, C., J. VANGRONSVELD, F. PORTEOUS, E.R.MOORE, S. TAGHAVI, M. MEZGEAY and D.V. DER LELIE, 2002. Endophytic bacteria and their potential applications. Critical Reviews in Plant Sciences 21: 583-606.
MA, Y., J. JIAO, X. FAN, H. SUN, Y. ZHANG, J. JIANG and C. LIU, 2017. Endophytic bacterium Pseudomonas fluorescens RG11 may transform tryptophan to melatonin and promote endogenous melatonin levels in the roots of four grape cultivars. Frontiers in Plant Science 7: 2068.
MARK, G.L., J. MORRISSEY, P. HIGGINS and F. OGARA, 2006. Molecular-based strategies to exploit Pseudomonas biocontrol strains for environmental biotechnology applications. FEMS Microbiology Ecology 56:167-177.
MARTINEZ, E., K. RODRIGUEZ and S .SANCHEZ, 2017. Endophytes as sources of antibiotics. Biochemical Pharmacology 134: 1-17.
MELO, F.M., M.F. FIORE, L.A. MORAES, M.E. SILVA-STENICO, S. SCRAMIN, M.D. TEIXEIRA and I.S. MELO, 2009. Antifungal compound produced by the cassava endophyte Bacillus pumilus MAIIIM4A. Scientia Agricola 66: 583-592.
MIAO, G.P., J. HAN, C. WANG, K.G. ZHANG and S.C. WANG, 2018. Growth inhibition and induction of systemic resistance against Pythium aphanidermatum by Bacillus simplex strain HS-2. Biocontrol Science and Technology 28: 1114-112.
MOSIMANN, C., T. OBERHANSLI, D. ZIEGLER, D. NASSAL, E. KANDELER, T. BOLLER and C. THONAR, 2017. Tracing of two Pseudomonas strains in the root and rhizoplane of maize, as related to their plant growth-promoting effect in contrasting soils. Frontiers in Microbiology 7: 2150.
NGOMA, L., B. ESAU and O. BABALOLA, 2013. Isolation and characterization of beneficial indigenous endophytic bacteria for plant growth promoting activity in Molelwane Farm, Mafikeng, South Africa. African journal of Biotechnology 12: 26.
PALMQVIST, N., S. BEJAI, J. MEIJER, G A. SEISENBAEVA and V.G.KESSLER, 2015. Nano titania aided clustering and adhesion of beneficial bacteria to plant roots to enhance crop growth and stress management. Scientific Reports 5: 10146.
PATTEN, C. and B. GLICK, 2002. Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Applied and Environmental Microbiology 68: 3795-3801.
PICARD, C. and M. BOSCO, 2008. Genotypic and phenotypic diversity in populations of plant-probiotic Pseudomonas spp. colonizing roots. Naturwissenschaften 95: 1-6.
PIKOVSKAYA, R., 1948. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17: 362-370.
PHETCHARAT, P. and A. Duangpaeng, 2012. Screening of endophytic bacteria from organic rice tissue for indole acetic acid production. Procedia Engineering 32: 177-183.
POPOVIC, T., M. IGNJATOV, D. JOSIC, M. STAROVIC, S. ZIVKOVIC, G. ALEKSIC and N. TRKULJA, 2012. Detekcija Xanthomonas axonopodis pv. Phaseoli Pseudomonas savastanoi pv. phaseolicola sa semena pasulja korišćenjem Milk-tween podloge. Field and Vegetable Crops Research/Ratarstvo i povrtarstvo 49:1.
RODRIGUES, A., M. FORZANI, R. SOARES, S. SIBOV and J.VIEIRA, 2016. Isolation and selection of plant growth-promoting bacteria associated with sugarcane. Pesquisa Agropecuária Tropical 46: 149-158.
RODRIGUEZ, H. and R. FRAGA, 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology Advances 17: 319-339.
RYAN, R.P., K .GERMAINE, A. FRANKS, D.L. RYAN and D.N. DOWLING, 2008. Bacterial endophytes: recent developments and applications. FEMS Microbiology Letters 278:1-9.
SAHARAN, B.S. and V. NEHRA, 2011. Plant growth promoting rhizobacteria: a critical review. Life Sciences and Medicine Research 21: 30.
SALLAM, N., 2011. Biological control of common blight of bean (Phaseolus vulgaris) caused by Xanthomonas axonopodis pv. Phaseoli by using the bacterium Rahnella aquatilis. Archives of Phytopathology and Plant Protection 44: 1966-1975.
SAFDARPOUR, F., 2017. Assessment of antagonistic and plant growth promoting activities of tomato endophytic bacteria in challenging with Verticillium dahliae under in-vitro and in-vivo conditions. Biological Journal of Microorganism 27: 77-90.
SARAVANAKUMAR, D. and R. SAMIYAPPAN, 2007. ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. Journal of Applied Microbiology 102: 1283-1292.
SCHAAD, N.W., J.B. JONES and W. CHUN, 2001. Laboratory guide for the identification of plant pathogenic bacteria. St Paul, USA, American Phytopathological Society (APS Press).American Phytopathological Society.
SCHMUTZ, J., P. MCCLEAN, S. MAMIDI, G. WU, S.CANNON, J. GRIMWOOD and C. CHAVARRO, 2014. A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genetics 46: 707.
SCHULZE, J., 2004. How are nitrogen fixation rates regulated in legumes. Journal of Plant Nutrition and Soil Science 167: 125-137.
SESSITSCH, A., J.HOWIESON, X. PERRET, H. ANTOUN and E. MARTINEZ-ROMERO, 2002. Advances in Rhizobium Research. Critical Reviews in Plant Sciences 21: 323-378.
SGROY, V., F. CASSAN, O. MASCIARELLI, M. DEL PAPA, A. LAGARES and V. LUNA, 2009. Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Applied Microbiology and Biotechnology 85: 371-381.
SHALINI, D., A. BENSON, R.GOMATHI, A. HENRY, S. JERRITTA and M. JOE, 2017. Isolation, characterization of glycolipid type biosurfactant from endophytic Acinetobacter sp. ACMS25 and evaluation of its biocontrol efficiency against Xanthomonas oryzae. Biocatalysis and Agricultural Biotechnology 11: 252-258.
SHARMA, S., R. SAYYED, M. TRIVEDI and T. GOBI, 2013. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springer Plus 2: 587.
SHEN, M., Y.J. KANG, H.L. WANG, X.S. ZHANG and Q.X. ZHAO, 2012. Effect of plant growth-promoting rhizobacteria (PGPRs) on plant growth, yield, and quality of tomato (Lycopersicon esculentum Mill.) under simulated seawater irrigation. The Journal of General and Applied Microbiology 58: 253-262.
SIDDIQUI, I.A. and S.S. SHAUKAT, 2002. Mixtures of plant disease suppressive bacteria enhance biological control of multiple tomato pathogens. Biology and Fertility of Soils 36: 260–268.
SOYLU, S., E.M SOYLU, S. KURT and O.K. EKICI, 2005. Antagonistic potentials of rhizosphere-associated bacterial isolates against soil-borne diseases of tomato and pepper caused by Sclerotinia sclerotiorum and Rhizoctonia solani. Asian Journal of Plant Sciences Res 2: 180-186.
STURZ, A.V., B.R. CHRISTIE and J. NOWAK, 2000. Bacterial Endophytes: Potential role in developing sustainable systems of crop production, critical reviews in plant sciences 19: 1-30.
SULTANA, R., S. ISLAM, A. ISLAM and B. SIKDAR, 2018. Identification of pathogen causing common bacterial blight (CBB) of bean through the biochemical and molecular pathway and their management system. Journal of Entomology and Zoology Studies.6: 652-757.
SUN, Z.B., X.F. YUAN, H. ZHANG, L.F. WU, C. LIANG and Y. J. FENG, 2013. Isolation, screening and identification of antagonistic downy mildew endophytic bacteria from cucumber. European Journal of Plant Pathology 4: 847-857.
TAMURA, K., D. PETERSON, N. PETERSON, G. STECHER, M. NEI and S. KUMAR, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
TASHI-OSHNOEI, F., B. HARIGHI and J. ABDOLLAHZADEH, 2017. Isolation and identification of endophytic bacteria with plant growth promoting and biocontrol potential from oak trees. Forest Pathology 47: 12360.
TARIQ, M., M. NOMAN, T. AHMED, A. HAMEED, N. MANZOOR and M. ZAFAR, 2017. Antagonistic features displayed by plant growth promoting rhizobacteria (PGPR): a review. Journal of Plant Science and Phytopathology 1: 38-43.
WANG, X., Q. LI, J. SUI, J. ZHANG, Z. LIU, J. DU, R. XU, Y. ZHOU and X. LIU, 2019. Isolation and characterization of antagonistic bacteria Paenibacillus jamilae HS-26 and their effects on plant growth. BioMed Research International 2019: 1-13.
YAZDANI-KHAMENEH, S., A. GOLNARAGHI and S.J. WYLIE, 2019. Diverse endophytic fungi colonize indigenous grasses in the Hyrcanian forest of Iran. In: Mleczko P (ed) The 18th Congress of European Mycologists, 16-21September 2019. Warsaw, Poland 220.
YANTI, Y., W. WARNITA, R. REFLIN and C.R. NASUTION, 2018. Characterizations of endophytic Bacillus strains from tomato roots as growth promoter and biocontrol of Ralstonia solanacearum. Biodiversitas 19: 906-911.
YOUNG, J.M., DC. PARK and B.S. WEIR, 2004. Diversity of 16S rRNA sequences of Rhizobium spp. implications for species determinations. FEMS Microbiology Letters 238: 125-131.
YOUSEFI, H., N. HASSANZADEH, K. BEHBOUDI and F.B. FIROUZJAHI, 2018. Identification and determination of characteristics of endophytes from rice plants and their role in biocontrol of bacterial blight caused by Xanthomonas oryzae pv. oryzae. Hellenic Plant Protection Journal 11:19–33.
YU, K., S. PARK and V. POYSA, 2000. Marker-assisted selection of common beans for resistance to common bacterial blight: efficacy and economics. Plant Breeding 119: 411-415.
YUAN, M., H. HE, L. XIAO, T. Zhong, H. LIU, S. LI and Y. JING, 2014. Enhancement of Cd phytoextraction by two Amaranthus species with endophytic Rahnella sp. JN27.Chemosphere 103: 99-104.
ZANATTA, Z., A. MOURA, L. MAIA and A. SANTOS, 2007. Bioassay for selection of biocontroller bacteria against bean common blight (Xanthomonas axonopodis pv. phaseoli). Brazilian Journal of Microbiology 38: 511-515.
ZHANG, H., M.S. KIM, V. KRISHNAMACHARI, P. PAYTON, Y. SUN, M. GRIMSON and I.S. MELO, 2007. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226: 839.
ZHU, Y., D. LU, M. LIRA, Q. XU, J. XIONG, M. MAO, H CHUNG and G. ZHENG, 2016. Droplet digital polymerase chain reaction detection of HER2 amplification in formalin fixed paraffin embedded breast and gastric carcinoma samples. Experimental and Molecular Pathology. 100: 287-293.
ZINNIEL, D., P. LAMBRECHT, N. HARRISN, Z. FENG, D. KUCZMARSKI, P. HIGLEY and A. VIDAVER, 2002. Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Applied and Environmental Microbiology 68: 2198-2208.
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