Abstract
Cronartium orientale is a heteroecious rust fungus that causes pine gall rust of two-needle pines, e.g., Japanese black pine (Pinus thunbergii) and Japanese red pine (Pinus densiflora). Basidiospores are discharged from telia on fagaceous plants, then infect pine shoots and/or stems. To determine the infection site of basidiospores on host plants, we inoculated 1–6-month-old seedlings of Japanese black pine and Japanese red pine. Seedlings with wounds formed by the removal of a few needles by a downward pull or by pruning a tip of the shoot produced galls more frequently than seedlings without wounds. When current-year shoots of 4-year-old Japanese black pine seedlings and new shoots from secondary buds induced by “Mekiri” treatment were inoculated after the removal of several needles from the seedlings, significantly more galls were produced than on shoots without wounds. Histological observations revealed that the germ tubes of basidiospores penetrated host cells exposed in the wounds, whereas basidiospores on the intact surface of needles and stems germinated directly or indirectly but did not invade host tissues. Thus, C. orientale basidiospores require fresh stem wounds for infection.
Similar content being viewed by others
References
Aime MC (2006) Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47:112–122
Anonymous (2014) Kuromatsu (Japanese black pine) bonsai. In: Learning from examples of bonsai tree care (in Japanese). Kindai-shuppan, Kyoto
Burdsal HH Jr, Snow GA (1977) Taxonomy of Cronartium quercuum and C. fusiforme. Mycologia 69:503–508
Colley RH (1918) Parasitism, morphology, and cytology of Cronartium ribicola. J Agric Res 15:619–659
EFSA Panel on Plant Health (EFSA PLH Panel) (2019) Commodity risk assessment of black pine (Pinus thunbergii Parl.) bonsai from Japan. EFSA J 17(5):5667
Farjon A (2005) Pines. Drawings and descriptions of the genus Pinus, 2nd edn. Brill, Leiden Netherlands
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Gold RE, Mendgen K (1991) Rust basidiospore germlings and disease initiation. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Springer, New York, pp 67–99
Hansen EM, Lewis KJ, Chastagner GA (2018) Compendium of conifer diseases, 2nd edn. APS Press, St. Paul
Hervé M (2020) RVAideMemoire: testing and plotting procedures for biostatistics. In: R package version 0.9-75. https://CRAN.R-project.org/package=RVAideMemoire
Hiratsuka N (1932) Inoculation experiments with some heteroecious species of the Melampsoraceae in Japan. Jpn J Bot 6:1–33
Hiratsuka N, Sato S (1984) Inoculation experiments with heteroecious species of the Japanese rust fungi (VI). Rept Tottori Mycol Inst (Jpn) 22:42–44
Hiratsuka N, Yoshida Y (1931) Heteroecism of Cronartium quercuum (in Japanese). J Plant Protect (Tokyo) 18:339–342
Hiratsuka N, Sato S, Katsuya K, Kakishima M, Hiratsuka Y, Kaneko S, Ono Y, Sato T, Harada Y, Hiratsuka T, Nakayama K (1992) The rust flora of Japan. In: Tsukuba Shuppankai, Tsukuba, Ibaraki, Japan
Hiratsuka Y, Powell JM (1976) Pine stem rusts of Canada. In: Canadian Forestry Service Forestry Technical Report 4, Northern Forest Research Centre, Edmonton, Alberta, Canada
Hirt RR (1938) Relation of stomata to infection of Pinus strobus by Cronartium ribicola. Phytopathology 28:180–190
Ito K (1974) Pathology of forest trees III (in Japanese). Norin Shuppan Co. Ltd, Tokyo
Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (eds) (1995) Flora of Japan, vol I. Pteridophyta and Gymnospermae. Kodansha Ltd., Tokyo
Japan Federation of Landscape Contractors (eds) (2008) Pearls of wisdom among gardeners (in Japanese). Kodansha Ltd., Tokyo, Japan
Kaneko S (2000) Cronartium orientale, sp. nov., segregation of the pine gall rust in eastern Asia from Cronartium quercuum. Mycoscience 41:115–122
Kondo H (1970) Pathogenicity of Cronartium quercuum on Fagaceae (in Japanese). In: Trans 81st Ann Mtg Jpn For Soc, pp 241–244
Kondo H (1975) Studies on eastern gall rust of pines (Cronartium quercuum (Berk.) Miyabe ex Shirai), with special reference to the life cycle, the infection period to pines, and pathogenic variability to alternate hosts of the causal fungus (in Japanese with English summary). Bull Ibaraki Pref For Exp Stat 8:1–107
Kondo H (1969) Inoculation experiments with teliospores of Cronartium quercuum on Pinus densiflora (in Japanese). In: Trans 80th Ann Mtg Jpn For Soc, pp 300–302
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Littlefield LJ, Heath MC (1979) Ultrastructure of rust fungi. Academic Press, New York
Miller T, Matthews FR (1984) Wounds on loblolly pines are sites of infection for fusiform rust fungus. South J Appl For 8:205–207
Miller T, Patton RF, Powers HR Jr (1980) Mode of infection and early colonization of slash pine seedlings by Cronartium quercuum f. sp. fusiforme. Phytopathology 70:1206–1208
Myrholm CL, Hiratsuka Y (1993) A new method for inoculating jack pine seedlings with the western gall rust fungus Endocronartium harknessii. Can J Plant Pathol 15:29–33
O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CABI, Wallingford, pp 225–233
Pappinen A, von Weissenberg K (1994) The ability of the pine-top weevil to carry spores and infect Scots pine with Endocronartium pini. Eur J For Pathol 24:258–263
Pappinen A, von Weissenberg K (1996) Weevil feeding on Scots pine affects germination of Endocronartium pini. Eur J For Pathol 26:225–234
Patton RF, Johnson DW (1970) Mode of penetration of needles of eastern white pine by Cronartium ribicola. Phytopathology 60:977–982
Patton RF, Nicholls TH (1966) Fluorescent labeling for observation of basidiospores of Cronartium ribicola on white pine needles. In: Gerhold HD, Schreiner EJ, McDermott RE, Winieski JA (eds) Breeding pest-resistant trees. Pergamon Press, Oxford, pp 153–162
Peterson RS, Jewell FF (1968) Status of American stem rusts of pine. Ann Rev Phytopathol 6:23–40
R Core Team (2019) R: a language and environment for statistical computing. In: R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/index.html
Sakuyama T (1979) Ecology and control of eastern gall rust on Japanese red pine (Pinus densiflora Sieb. et Zucc.) caused by Cronartium quercuum (Berk.) Miyabe ex Shirai (in Japanese with English summary). Bull Iwate Pref For Expt Stat 3:21–49
Shirai M (1899) On the genetic connection between Peridermium giganteum (Mayr) Tubeuf and Cronartium quercuum (Cooke) Miyabe. Bot Mag (Tokyo) 13:74–79
Shukla AN, Schmidt RA, Miller T (2001) Symptoms in slash pine seedlings following inoculation with the cone rust fungus Cronartium strobilinum. For Pathol 31:345–352
Sinclair WA, Lyon HH (2005) Diseases of trees and shrubs, 2nd edn. Cornell University Press, Ithaca
Van Arsdel EP (1968) Stem and needle inoculations of eastern white pine with the blister rust fungus. Phytopathology 58:512–514
Vilgalys R, Hester M (1990) Rapid genetic identification and map** of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
Acknowledgements
This research was supported by grants from the Project of the NARO Bio-oriented Technology Research Advancement Institution (the special scheme project on vitalizing management entities of agriculture, forestry, and fisheries) (Grant no. 16932591). We thank the Sugadaira Research Station, Mountain Science Center, University of Tsukuba, Japan, for providing experimental materials. We thank Dr. Kaoru Yamaguchi, Biological Resource Center (NBRC), National Institute of Technology and Evaluation, for her support in preparing specimens for SEM. Part of this study was presented at the 2020 Annual Meeting of the Phytopathological Society of Japan.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
10327_2022_1054_MOESM1_ESM.jpeg
Fig. S1. Japanese black pine seedlings used for inoculation. a: Seedling without “Mekiri” treatment on 29 June 2019. B: Seedling after “Mekiri” treatment on 29 June 2019. c: Seedling forming new shoots from secondary buds (arrow head) 28 d after “Mekiri” treatment. d: Seedling after “Tochu-Mekiri” treatment on 6 July 2019. e: Seedling forming new shoots from secondary buds (arrow head) 28 d after “Tochu-Mekiri” treatment. CS: current-year shoot. Arrows indicate cut end of current-year shoots (JPEG 956 kb)
10327_2022_1054_MOESM2_ESM.jpeg
Fig. S2. Orangish-yellow aeciospores produced on galls 776 days (a) and 596 days (b) after inoculation. a: Gall on same Japanese red pine seedling shown in Fig. 2a–d. b: Gall on same Japanese black pine seedling shown in Fig. 3d–f (JPEG 447 kb)
10327_2022_1054_MOESM3_ESM.docx
Fig. S3. Alignment of sequence data from 12 galls and C. orientale (LC585374 and MK193821). Codes for the sample used in this study are in parentheses (DOCX 1638 kb)
Rights and permissions
About this article
Cite this article
Yamaoka, Y., Okane, I., Suzuki, H. et al. Infection through wounds on shoots of pine seedlings by basidiospores of Cronartium orientale. J Gen Plant Pathol 88, 161–172 (2022). https://doi.org/10.1007/s10327-022-01054-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10327-022-01054-9