Abstract
Huanglongbing (HLB) is the main disease of citriculture worldwide, being mainly caused by the bacterium known as ‘Candidatus Liberibacter asiaticus’ (CLas), limited to the phloem and naturally transmitted by vector insects known as psyllids. For the production of citrus seedlings, it is necessary to use rootstocks that are propagated by seeds from fruits produced by mother plants grown in field, however being submitted to natural HLB transmission. Although there is no evidence of CLas transmission from seeds to seedlings, little is known about the effects of this bacterium on the physiological quality of seeds obtained from CLas-infected plants. Therefore, the aim of this work was to evaluate the physiological quality of seeds from ‘Rangpur’ lime and ‘Swingle’ citrumelo rootstocks, from CLas-infected plants, with symptomatic and asymptomatic branches. The parameters evaluated, in addition to fruit development in mother plants, were germination rate, tetrazolium test, electrical conductivity, seedling emergence in greenhouse, and vegetative development and molecular analysis via qPCR for the detection of bacteria (leaf petiole, fruit peduncles, roots, seed coats, and seed endosperm). The presence of CLas in plants of both rootstocks has negative impact on fruit development, as well as on the number of normal seeds. In addition, there is reduced germination and seed emergence. Although CLas was detected in different tissues (leaf petiole, fruit peduncles and seed coat, and seed embryo), no vertical bacteria transmission was detected. Results have shown that seeds from CLas-infected branches have impaired physiological quality, but without bacterial transmission from seeds to seedlings.
References
Albrecht U, Bowman KD (2009) Candidatus Liberibacter asiaticus and Huanglongbing effects on citrus seeds and seedlings. Hortscience 44:1969–1972
Association of Official Seed Analysts - AOSA (1983) Seed vigor testing handbook (contribution 32). AOSA, New York
Barbosa MR, Silva CB, Medeiros MA, Centurion APPC, Vieira RD (2012) Condutividade elétrica em função do teor de água inicial de sementes de amendoim. Ciência Rural 42:45–51
Bassanezi RB, Montesino LH, Stuchi ES (2009) Effects of Huanglongbing on fruit quality of sweet orange cultivars in Brazil. European Journal of Plant Pathology 125:565–557
Beloti VH, Alves GR, Coletta-Filho HD, Yamamoto PT (2018) The Asian citrus psyllid host Murraya koenigii is immune to citrus huanglongbing pathogen ‘Candidatus Liberibacter asiaticus’. Phytopathology 108:1089–1094
Bové JM (2016) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88:7–37
Brasil (2009) Ministério da Agricultura, Pecuária e Abastecimento. Regras para análise de sementes. Secretaria Nacional de Defesa Agropecuária, Brasília
Camara RC, Vigo SC, Maringoni AC (2009) Plant-toseed transmission of Curtobacterium flaccumfaciens pv. flaccumaciens in a dry bean cultivar. Journal of Plant Pathology, 91:549–554
Carvalho NM, Nakagawa J (2000) Sementes: ciência, tecnologia e produção. 4th Ed. Funep, Jaboticabal
Chapot H. (1975) The citrus plant. In: Hafliger E (Ed.) Citrus. Ciba-Geigy Agrochemicals, Switzerland. pp. 6–13
Chen J, Pu X, Deng X, Liu S, Li H, Civerolo E (2009) A phytoplasma related to ‘Candidatus Phytoplasma asteri’ detected in citrus showing Huanglongbing (yellow shoot disease) symptoms in Guangdong, P.R. China. Phytopathology 99:236–242
Coletta-Filho DH, Alves Carvalho S, Carvalho Silva LF, Machado MA (2014) Seven years of negative detection results confirm that Xylella fastidiosa, the causal agent of CVC, is not transmitted from seeds to seedlings. European Journal of Plant Pathology 139:593–596
Duarte FEVO, Barros DR, Girardi EA, Filho WSS, Passos OS (2013) Poliembrionia e atributos morfológicos de sementes de porta-enxertos de citros. Revista Brasileira de Fruticultura 35:246–254
Etxeberria E, Gonzalez P, Achor D, Albrigo G (2009) Anatomical distribuction of abnormally high levels of starch in HLB-affected Valencia orange trees. Physiological and Molecular Plant Pathology 74:76–83
Fan J, Chen C, Blansky RH, Gmitter FG, Li ZG (2010) Changes in carbohydrate metabolism in Citrus sinensis infected with ‘Candidatus Liberibacter asiaticus’. Plant Pathology 59:1037–1043
França-Neto JB, Krzyzanowski FC, Henning AA (2011) Qualidade da semente de soja e sua importância na produtividade. Boletim de Pesquisa de Soja da Fundação MT 15:424–428
Gottwald TR, Gracxa JV, Bassanezi RB (2007) Citrus huanglongbing: the pathogen and its impact. Plant Health Progress. Online publication 1–35
Gottwald TR, Graham JH, Irey MS, Mccollum TG, Wood BW (2012) Inconsequential effect of nutritional treatments on huanglongbing control, fruit quality, bacterial titer and disease progress. Crop Protection 36:73–82
Graham JH, Irey MS, Dawson WO, Hall D, Duan Y (2008) Assessment of transmission of Liberibacter asiaticus from seed to seedlings of ‘Pineapple’ sweet orange and Carrizo citrange. In: proceedings of International Research Conference on Huanglongbing 174p
Halbert SE, Manjunath KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Florida Entomologist 87:330–353
Hartung JS, Halbert SE, Pelz-Stelinski K, Brlansky RH, Chen C, Gmitter FG (2010) Lack of evidence for transmission of ‘Candidatus Liberibacter asiaticus’ through citrus seed taken from affected fruit. Plant Disease 10:1200–1205
Hilf ME (2011) Colonization of citrus seed coats by ‘Candidatus Liberibacter asiaticus’: implications for seed transmission of the bacterium. Phytopathology 101:1242–1250
Lopes AS, Frare GF, Bertolini E, Cambra M, Fernandes NG, Marin DR, Bové M (2009) Liberibacters associated with citrus huanglongbing in Brazil: ‘Candidatus Liberibacter asiaticus’ is heat tolerant, ‘Ca. L. americanus’ is heat sensitive. Plant Disease 93:257–262
Lou BR, Zhao XL, Song YQ, Bai XJ, Deng CL, Chen GP (2012) “Candidatus Liberibacter asiaticus”, associated with citrus Huanglongbing, infects pollen, seed coat and endosperm of pummelo in China. Journal of Plant Pathology 94:703–705
Moreira RA, Ramos JD, Cruz MCM (2010) Caracterização de frutos e poliembrionia em sementes de ‘Flying Dragon’ e de híbridos de porta-enxerto de citros. Revista Brasileira de Fruticultura 32:327–345
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 239:487–491
Schneider H (1968) Anatomy of greening-diseased sweet orange shoots. Phytopathology 58:262–266
Shokrollah H, Abdullah TL, Sijam K, Abdullah SNA (2009) Determination of the presence of Huanglongbing in seeds and movement of the pathogen in Citrus reticulata. American Journal of Applied Sciences 6:1180–1185
Tatineni SU, Shankar Sagaram S, Gowda CJ, Robertson WO, Dawson T, Iwanami Wang N (2008) In planta distribution of ‘Candidatus Liberibacter asiaticus’ as revealed by polymerase chain reaction (PCR) and real-time PCR. Phytopathology 98:592–599
Van Vuuren SP, Cook G (2011) Lack of evidence for seed transmission of ‘Candidatus Liberibacter africanus’ associated with greening (Huanglongbing) in citrus in South Africa. Plant Disease 95:1026–1026
Wang N, Trivedi P (2013) Citrus Huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 103:652–665
Xu X, Miller SA, Baysal-Gurel F, Gartemann KH, Eichenlaub R, Rajashekara G (2010) Bioluminescence imaging of Clavibacter michiganensis subsp. michiganensis infection of tomato seeds and plants. Applied and Environmental Microbiology 76:3978–3988
Zheng Z, Bao M, Wu F, Van Horn C, Chen J, Deng X (2018) A type 3 prophage of ‘Candidatus Liberibacter asiaticus’ carrying a restriction-modification system. Phytopathology 108:454–461
Zucoloto M, Costa MG, Carvalho LM, Santos D, Siqueira DL (2011) Estimativa da produção de sementes de porta-enxertos cítricos por meio da massa de frutos. Revista Ceres 58:126–128
Acknowledgements
M. Morelli acknowledges Capes, Brazil (process: 1368040)) for fellowship granted. FA Azevedo and HD Coletta Filho acknowledge CNPq, Brazil for fellowships granted.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Morelli, M., Takayassu, F.H., de Andrade Pacheco, C. et al. Impact of HLB on the physiological quality of citrus rootstock seeds and non-vertical ‘Candidatus Liberibacter asiaticus’ transmission. Trop. plant pathol. 45, 620–625 (2020). https://doi.org/10.1007/s40858-020-00371-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40858-020-00371-8