Impact of HLB on the physiological quality of citrus rootstock seeds and non-vertical ‘Candidatus Liberibacter asiaticus’ transmission

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.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. Albrecht U, Bowman KD (2009) Candidatus Liberibacter asiaticus and Huanglongbing effects on citrus seeds and seedlings. Hortscience 44:1969–1972

    Article  Google Scholar 

  2. Association of Official Seed Analysts - AOSA (1983) Seed vigor testing handbook (contribution 32). AOSA, New York

  3. 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

    Article  Google Scholar 

  4. 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

  5. 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

    CAS  Article  Google Scholar 

  6. Bové JM (2016) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88:7–37

    Google Scholar 

  7. Brasil (2009) Ministério da Agricultura, Pecuária e Abastecimento. Regras para análise de sementes. Secretaria Nacional de Defesa Agropecuária, Brasília

  8. 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

  9. Carvalho NM, Nakagawa J (2000) Sementes: ciência, tecnologia e produção. 4th Ed. Funep, Jaboticabal

  10. Chapot H. (1975) The citrus plant. In: Hafliger E (Ed.) Citrus. Ciba-Geigy Agrochemicals, Switzerland. pp. 6–13

  11. 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

    CAS  Article  Google Scholar 

  12. 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

    CAS  Article  Google Scholar 

  13. 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

  14. 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

    CAS  Article  Google Scholar 

  15. 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

    CAS  Article  Google Scholar 

  16. 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

  17. Gottwald TR, Gracxa JV, Bassanezi RB (2007) Citrus huanglongbing: the pathogen and its impact. Plant Health Progress. Online publication 1–35

  18. 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

    Article  Google Scholar 

  19. 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

  20. 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

    Article  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. Hilf ME (2011) Colonization of citrus seed coats by ‘Candidatus Liberibacter asiaticus’: implications for seed transmission of the bacterium. Phytopathology 101:1242–1250

    Article  Google Scholar 

  23. 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

  24. 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

    Google Scholar 

  25. 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

    Article  Google Scholar 

  26. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 239:487–491

    Google Scholar 

  27. Schneider H (1968) Anatomy of greening-diseased sweet orange shoots. Phytopathology 58:262–266

    Google Scholar 

  28. 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

    CAS  Article  Google Scholar 

  29. 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

    CAS  Article  Google Scholar 

  30. 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

    Article  Google Scholar 

  31. Wang N, Trivedi P (2013) Citrus Huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 103:652–665

    Article  Google Scholar 

  32. 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

    CAS  Article  Google Scholar 

  33. 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

    Article  Google Scholar 

  34. 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

    Article  Google Scholar 

Download references

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

Affiliations

Authors

Corresponding author

Correspondence to Fernando Alves de Azevedo.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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. (2020). https://doi.org/10.1007/s40858-020-00371-8

Download citation

Keywords

  • Bacterium
  • Citrus
  • Greening
  • ‘Rangpur’ lime
  • ‘Swingle’ citrumelo
  • Seeds