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Role of lenticels and microcracks on susceptibility of apple fruit to Botryosphaeria dothidea

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Abstract

Apple ring rot, caused by Botryosphaeria dothidea, is one of the most serious diseases affecting apple industry in East Asia. To study the correlation between fruit natural exocarp structures and susceptibility to B. dothidea, lesion length of Malus domestica cultivars and Malus germplasm accessions was measured 14 days after in vitro inoculation with B. dothidea mycelia at different developmental stages. Area per fruit surface (APFS) of lenticels and microcracks and thickness of cuticular wax were observed. Lesion length, lenticel APFS and cuticular wax thickness varied significantly among the 11 cultivars studied. A positive correlation between lesion length and lenticel APFS and a negative correlation between lesion length and cuticular wax thickness were detected among cultivars and during fruit development. In addition, similar correlations were validated in nine Malus germplasm accessions. Numerous microcracks were observed on surfaces of Golden Delicious and Golden Spur fruit, accounting for 90 % of the natural openings. The hyphae of B. dothidea penetrated into exocarp through both lenticels and microcracks. Fruit bagging with double-layered paper bags and exogenous GA4+7 reduced lenticel APFS, thickened cuticular wax and elevated resistance to disease. Natural openings on fruit exocarp are an important factor affecting susceptibility of apple to B. dothidea.

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Abbreviations

APFS:

Area per fruit surface

DAFB:

Days after full bloom

LM:

Light microscopy

SEM:

Scanning electron microscopy

References

  • Belding, R. D., Blankenship, S. M., Young, E., & Leidy, R. B. (1998). Composition and variability of epicuticular waxes in apple cultivars. Journal of the American Society for Horticultural Science, 123, 348–356.

    CAS  Google Scholar 

  • Brown, E. A., & Britton, K. O. (1986). Botryosphaeria diseases of apple and peach in southeastern United States. Plant Disease, 70(5), 480–484.

    Article  Google Scholar 

  • Brown, E. A., & Hendrix, F. F. (1981). Pathogenicity and histopathology of Botryosphaeria dothidea on apple stems. Phytopathology, 71, 375–379.

    Article  Google Scholar 

  • Chen, Z., Wang, Y., & Yin, S. (1992). A study on the mechanism of resistance to sheath blight in rice. Scientia Agricultura Sinica, 25(4), 41–46.

    Google Scholar 

  • Chen, J., Sheng, B., & Liu, K. (1995). Mechanism of apple varieties resistat to lenticel infection by ring rot. Proceedings of Horticultural Society, 94–100.

  • Conway, W. S. (1992). Calcium treatment and postharvest rot on apple and potato. Plant Disease, 76(4), 329–333.

    Article  CAS  Google Scholar 

  • Curry, E. (2008). Effects of 1-MCP applied postharvest on epicuticular wax of apples (Malus domestica Borkh.) during storage. Journal of the Science of Food and Agriculture, 88, 996–1006.

    Article  CAS  Google Scholar 

  • Curry, E. A., Torres, C., & Neubauer, L. (2008). Preharvest lipophilic coatings reduce lenticel breakdown disorder in ‘Gala’ apples. HortTechnology, 18(4), 690–696.

    CAS  Google Scholar 

  • Eccher, T., & Boffelli, G. (1981). Effects of dose and time of application of GA4+7 on russeting, fruit set and shape of ‘Golden Delicious’ apples. Scientia Horticulturae, 14, 307–314.

    Article  Google Scholar 

  • Ende, G. V. D. (1974). Cutinolytic enzymes in relation to pathogenesis. Annual Review of Phytopathology, 12, 247–258.

    Article  Google Scholar 

  • Espelie, K. E. (1980). Composition of suberin-associated waxes from the subterranean storage organs of seven plants. Planta, 148, 468–476.

    Article  CAS  PubMed  Google Scholar 

  • Faust, M., & Shear, C. B. (1972). Fine structure of the fruit surface of three apple cultivars. Journal of the American Society for Horticultural Science, 97, 351–355.

    Google Scholar 

  • Grimm, E., Khanal, B. P., Winkler, A., Knoche, M., & Köpcke, D. (2012). Structural and physiological changes associated with the skin spot disorder in apple. Postharvest Biology and Technology, 64(1), 111–118.

    Article  CAS  Google Scholar 

  • Guo, L., Li, J., Li, B., Zhang, X., Zhou, Z., Li, G., et al. (2009). Investigations on the occurrence and chemical control of Botryosphaeria canker of apple in China. Plant Protection, 35(4), 120–123.

    Google Scholar 

  • Han, J. W., Lee, H. J., Jang, H. I., Hong, K. H., Choi, J. J., Kim, K. Y., et al. (1999). Comparison of skin characteristics between non-bagged and bagged ‘Hosui’ pear (Pyrus pyrifolia Nakai) fruits. Journal of the Korean Society for Horticultural Science, 40(4), 439–442.

    Google Scholar 

  • Hao, Y., Zhao, Q., Liu, Q., & Li, W. (2011). Effects of them micro-environment inside fruit bags on the structure of fruit peel in ‘Fuji’ apple. Acta Ecologica Sinica, 31(10), 2831–2836.

    Google Scholar 

  • Harker, F. R., & Ferguson, I. B. (1988). Transport of calcium across cuticles isolated from apple fruit. Scientia Horticulturae, 36, 205–217.

    Article  Google Scholar 

  • Heather, W. A. (1969). Susceptibility of the juvenile leaves of Eucaluplus eucalypti (Hansf) Walker. Australian Journal of Biological Science, 20(4), 769–775.

    Google Scholar 

  • Kim, S. B., & Kim, S. C. (1989). Pathogenicity and ecology of apple rot caused by Botryosphaeria dothidea III. The comparison to resistance against apple rot among several cultivars. Journal of the Korean Society for Horticultural Science, 30(3), 207–214.

  • Kim, K. W., Kim, K. R., & Park, E. W. (2005). An infection model of apple white rot based on conidial germination and appressorium formation of Botryosphaeria dothidea. Plant Pathology Journal, 21, 322–327.

    Article  Google Scholar 

  • Knoche, M., Khanal, B. P., & Stopar, M. (2011). Russeting and microcracking of ‘Golden Delicious’ apple fruit concomitantly decline due to Gibberellin A4+7 application. Journal of the American Society for Horticultural Science, 136(3), 159–164.

    CAS  Google Scholar 

  • Konarska, A. (2012). Differences in the fruit peel structures between two apple cultivars during storage. Acta Scientiarum Polonorum-Hortorum Cultus, 11(2), 105–116.

    Google Scholar 

  • Li, G., Shen, Y., Gao, Y., Li, X., Gao, S., Wang, J., et al. (2004). Study on the relationship between lenticel tissue structure and density and the occurrence of apple rough bark disease. Journal of Fruit Science, 21(4), 350–353.

    Google Scholar 

  • Li, G., Gao, Y., Yang, H., Liu, X., Sun, L., & Wang, J. (2005). Observation of infection approach of Botryosphaeria berengriana f. piricola on apple stem under scanning electron microscope. Journal of Fruit Science, 22(2), 169–171.

    CAS  Google Scholar 

  • Li, G., Shen, Y., Gao, Y., Chen, J., & Yan, Z. (2006). Infection process of Botryosphaeria dothidea in apple fruit. Journal of Fruit Science, 23(1), 69–72.

    Google Scholar 

  • Li, C., Li, C., Zhang, X., & Huo, J. (2009). Advances in research on mechanism of apple resistance to ring rot disease and breeding. China Fruits, 3, 46–49.

    CAS  Google Scholar 

  • Li, F., Zhang, X., Yao, Y., Sun, X., & Liu, L. (2011). Whole fruit staining with aniline blue at harvest is associated with superficial pathogenesis of “Fuji” apples after storage. Biotechnic & Histochemistry, 86(6), 394–403.

    Article  CAS  Google Scholar 

  • Liang, X., Zhou, G., & Pan, R. (2003). Wax and cuticle of peanut seed coat in relation to infection and afiatoxin production by Asperillus flavus. Journal of Tropical and Subtropical Botany, 11(1), 11–14.

    CAS  Google Scholar 

  • Liu, H., Li, C., Fan, Y., & Hou, B. (2003). Correlative analysis of resistance-related factors in apple fruits to apple fruit ring rot disease. Journal of Agricultural University of Hebei, 26(1), 56–60.

    Google Scholar 

  • Liu, D., Zeng, Q., Ji, Q., Liu, C., Liu, S., & Liu, Y. (2012). A comparison of the ultrastructure and composition of fruits cuticular wax from the wild-type ‘Newhall’ navel orange (Citrus sinensis [L.] Osbeck cv. Newhall) and its glossy mutant. Plant Cell Reports, 31, 2239–2246.

    Article  CAS  PubMed  Google Scholar 

  • Mendgen, K., Schneider, A., Sterk, M., & Fink, W. (1988). The differentiation of infection structures as a result of recognition events between some biotrophic parasites and their hosts. Journal of Phytopatholohy, 123(3), 259–272.

    Article  Google Scholar 

  • Peng, Y., & Zhang, D. (2000). Ultrastructure of epidermis and flesh of the developing apple fruit. Acta Botanica Sinica, 42(8), 794–802.

    Google Scholar 

  • Prusky, D., Fuchs, Y., & Yanko, U. (1983). Assessment of latent infections as a basis for control of post-harvest disease of mango. Plant Disease, 67(7), 816–818.

    Article  Google Scholar 

  • Roy, S., Conway, W. S., Watada, A. E., Sams, C. E., Erbe, E. F., & Wergin, W. P. (1994a). Heat treatment affects epicuticular wax structure and postharvest calcium uptake in ‘Golden Delicious’ apples. HortScience, 29(9), 1056–1058.

    Google Scholar 

  • Roy, S., Watada, A. E., Conway, W. S., Erbe, E. F., & Wergin, W. P. (1994b). Low-temperature scanning electron microscopy of frozen hydrated apple tissues and surface organisms. HortScience, 29, 305–309.

    Google Scholar 

  • Roy, S., Conway, W. S., Watada, A. E., Sams, C. E., Erbe, E. F., & Wergin, W. P. (1999). Changes in the ultrastructure of the epicuticular wax and postharvest calcium uptake in apples. HortScience, 34(1), 121–124.

    CAS  Google Scholar 

  • Sun, Y., Yu, Q., & Xu, J. (2011). Relationship between lenticel tissue structure and the resistance to Botryosphaeria berengeriana f. piricola on apple stem. Journal of Agricultural University of Hebei, 34(06), 55–59.

    Google Scholar 

  • Tang, W., Ding, Z., Zhou, Z., Wang, Y., & Guo, L. (2012). Phylogenetic and pathogenic analyses show that the causal agent of apple ring rot in china is Botryosphaeria dothidea. Plant Disease, 96(4), 486–496.

    Article  Google Scholar 

  • Turketti, S. S., Curry, E., & Lötze, E. (2012). Role of lenticel morphology, frequency and density on incidence of lenticel breakdown in ‘Gala’ apples. Scientia Horticulturae, 138, 90–95.

    Article  Google Scholar 

  • Veraverbeke, E. A., Verboven, P., Oostveldt, P. V., & Nicola, B. M. (2003). Prediction of moisture loss across the cuticle of apple (Malus sylvestris subsp. mitis (Wallr.)) during storage. Postharvest Biology and Technology, 30(1), 75–88.

    Article  Google Scholar 

  • Wilson, C. L., Pusey, P. L., & Otto, B. E. (1981). Plant epidermal sections and imprints using cyanoacrylate adhesives. Canadian Journal of Plant Science, 61, 781–783.

    Article  Google Scholar 

  • Yan, Z., Zhang, Q., Zhang, S., Zhou, Z., Guo, G., & Wang, Z. (2005). Identification of apple cultivars for their resistance to ring rot disease. Journal of Fruit Science, 22(6), 654–657.

    Google Scholar 

  • Yang, L., Zhuang, Y., Wang, Y., Zhang, X., & Han, Z. (2012). The ultrastructural changes of apple fruit with different resistance infected by Botryosphaeria dothidea. Acta Horticulturae Sinica, 39(5), 963–969.

    Google Scholar 

  • Zhang, H., Wang, S., Mou, Q., Jiang, M., & Sun, F. (1996). Effect of bagging on the peel structure and PPO, POD activity of Pyrus bretschneideri. Acta Horticulturae Sinica, 23(1), 23–26.

    Google Scholar 

  • Zhang, Y., Wang, K., Wang, Y., Han, Z., Gao, Y., Xu, X., et al. (2010). Evaluation of resistance to fruit ring rot for apple germplasms. Acta Horticulturae Sinica, 37(4), 539–546.

    Google Scholar 

  • Zhuang, Y., Liu, H., Li, C., Wang, Y., Zhao, Y., Chen, D., et al. (2011). Inheritance of and molecular markers for susceptibility of Malus domestica. Journal of Phytopathology, 159, 782–788.

    Article  Google Scholar 

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Acknowledgments

This project was supported by the National High-Tech R&D Program of China (2011AA001204) and the Key Laboratory of Beijing Municipality of Stress Physiology and Molecular Biology for Fruit Trees.

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Conflict of Interest

The authors declare that they have no conflict of interest. The authors also state that a) the paper has not been previously published and is not under consideration by another journal; b) that all authors have agreed with the contents of the manuscript and its submission to this journal; c) all authors listed have contributed significantly to the work and agree to be in the author list.

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Authors and Affiliations

  1. Institute for Horticultural Plants, China Agricultural University, Beijing, 100193, China

    Yeqing Guan, Yi Wang, Ting Wu, Zhenhai Han & Xinzhong Zhang

  2. Changli Institute of Pomology, Hebei Academy of Agriculture and Forestry Sciences, Changli, 066600, China

    Ruifeng Chang & Guojian Liu

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  1. Yeqing Guan
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Correspondence to Xinzhong Zhang.

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Guan, Y., Chang, R., Liu, G. et al. Role of lenticels and microcracks on susceptibility of apple fruit to Botryosphaeria dothidea . Eur J Plant Pathol 143, 317–330 (2015). https://doi.org/10.1007/s10658-015-0682-z

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