Skip to main content
SpringerLink
Log in

Characterization of a novel fungal disease that infects the gametophyte of Pyropia yezoensis (Bangiales, Rhodophyta)

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

This study investigated a new fungal disease that attacks Pyropia yezoensis, an economically important red alga that is extensively cultured in China. An incidence was found in a P. yezoensis farm during mid to end November 2012 at Haizhou Bay, Jiangshu Province, China. Histopathology revealed that the naturally infected thalli were overwhelmed by a fungus, leading to progressive red rot symptoms. The causative agent was isolated, grown in pure culture, and identified as a member of the genus Alternaria by morphology and sequence analysis of the nuclear ribosomal DNA containing the internal transcribed spacer (ITS) region of ITS1 and ITS2. In artificial infection experiments on P. yezoensis blades, the fungal isolate was able to cause the same characteristic histopathology seen in natural infections. This fungal isolate grew well at a wide range of temperatures (8–36 °C) and at low salinities (5–50 ‰). In an orthogonal test used to determine the effects of environmental factors (temperature, salinity, and conidia concentration) on disease expansion, it was found that higher temperatures and lower salinities easily caused red rot disease, with the optimal conditions for disease development being 23 °C, 24 ‰ salinity, and a conidia concentration of 105 mL−1. This is the first report to show that Alternaria causes red rot disease in P. yezoensis.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arasaki S (1947) Studies on the rot of Porphyra tenera by a Pythium. Bull Jpn Soc Sci Fish 13:74–90

    Article  Google Scholar 

  • Arasaki S, Inouye A, Kochi Y (1960) The disease of the cultured Porphyra, with special reference to the cancer-disease and the chytrid-disease which occurred at the culture field in Tokyo Bay during 1959–1960. Bull Jpn Soc Sci Fish 26:1074–1079

    Article  Google Scholar 

  • Berto P, Comménil P, Belingheri L, Dehorter B (1999) Occurrence of a lipase in spores of Alternaria brassicicola with a crucial role in the infection of cauliflower leaves. FEMS Microbiol Lett 180:83–189

    Article  Google Scholar 

  • Blouin NA, Brodie JA, Grossman AC, Xu P, Brawley SH (2011) Porphyra: a marine crop shaped by stress. Trends Plant Sci 16:29–37

    Article  CAS  PubMed  Google Scholar 

  • Correa JA (1997) Infectious diseases of marine algae: current knowledge and approaches. Progr Phycol Res 12:139–145

    Google Scholar 

  • Ding HY, Ma JH (2005) Simultaneous infection by red rot and chytrid diseases in Porphyra yezoensis Ueda. J Appl Phycol 17:51–56

    Article  Google Scholar 

  • Eshel D, Miyara I, Ailing T, Dinoor A, Prusky D (2002) pH regulates endoglucanase expression and virulence of Alternaria alternate in persimmon fruit. Mol Plant-Microbe Interact 15:774–779

    Article  CAS  PubMed  Google Scholar 

  • Fan CY, Köller W (1998) Diversity of cutinases from plant pathogenic fungi: differential and sequential expression of cutinolytic esterases by Alternaria brassicicola. FEMS Microbiol Lett 158:33–38

    Article  CAS  Google Scholar 

  • Fujita Y (1990) Diseases of cultivated Porphyra in Japan. In: Akatsuka I (ed) Introduction to applied phycology. SPB, The Hague, The Netherlands, pp 177–190

  • Fujita Y, Zenitani B (1976) Studies on pathogenic Pythium of laver red rot in Ariake sea farm: I. General mycological characteristic. Nippon Suisan Gakkaishi 42:1183–1188

    Article  Google Scholar 

  • Gachon CM, Sime-Ngando T, Strittmatter M, Chambouvet A, Kim GH (2010) Algal diseases: spotlight on a black box. Trends Plant Sci 15:633–640

    Article  CAS  PubMed  Google Scholar 

  • Guan XY, Li J, Zhang Z, Li FC, Yang R, Jiang P, Qin S (2013) Characterizing the microbial culprit of white spot disease of the conchocelis stage of Porphyra yezoensis (Bangiales, Rhodophyta). J Appl Phycol 25:1341–1348

    Article  CAS  Google Scholar 

  • Guiry MD, Guiry GM (2014) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. http://www.algaebase.org

  • Kawamura Y, Yamashita Y, Kito H (1991) Growth of Porphyra yezoensis f. narawaensis on culture nets in the nori farm and its environmental conditions. Suisanzoshoku 39:273–278

    Google Scholar 

  • Kazama FY, Fuller MS (1973) Mineral nutrition of Pythium marium, a marine facultative parasite. Can J Bot 51:693–699

    Article  CAS  Google Scholar 

  • Kerwin JL, Johnson LM, Whisler HC, Tuininga AR (1992) Infection and morphogenesis of Pythium marinum in species of Porphyra and other red algae. Can J Bot 70:1017–1024

    Article  Google Scholar 

  • Kim MY, Sohn JH, Ahn JS, Oh H (2009) Alternaramide, a cyclic depsipeptide from the marine-derived fungus Alternaria sp SF-5016. J Nat Prod 72:2065–2068

    Article  CAS  PubMed  Google Scholar 

  • Ma JH (1992) Investigation research of the chytrid disease in Porphyra yezoensis Ueda along south coast of Jiangsu. J Shanghai Fish Univ 5(1):1–7

    Google Scholar 

  • Ma JH (1996) A preliminary study on the red rot disease of Porphyra yezoensis Ueda. J Shanghai Fish Univ 5(1):1–7

    CAS  Google Scholar 

  • MacArtain P, Gill CI, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543

    Article  PubMed  Google Scholar 

  • Mamgain A, Roychowdhury R, Tah J (2013) Alternaria pathogenicity and its strategic controls. Res J Biol 1:1–9

    Google Scholar 

  • Migita S (1973) Studies on chytrid blight disease of Porphyra. In: Japanese Society of Fisheries Science (ed) The disease of cultivated Porphyra. Koseisha Koseikaku, Tokyo, Japan, pp 12–20

  • Morrice LM, McLean MW, Long WF, Williamson FB (1983) Porphyran primary structure. Eur J Biochem 133:673–684

    Article  CAS  PubMed  Google Scholar 

  • Niu C, Kebede H (2008) A safe inexpensive method to isolate high quality plant and fungal DNA in an open laboratory environment. Afr J Biotechnol 7:2818–2822

    CAS  Google Scholar 

  • Noda H (1993) Health benefits and nutritional properties of Nori. J Appl Phycol 5:255–258

    Article  Google Scholar 

  • Park CS, Kakinuma M, Amano H (2006) Forecasting infections of the red rot disease on Porphyra yezoensis Ueda (Rhodophyta) cultivation farms. J Appl Phycol 18:295–299

    Article  Google Scholar 

  • Provasoli L (1968) Media and products for the cultivation of marine algae. In: Watarabe A, Hattori A (eds) Cultures and collections of algae. Jpn Soc Plant Physiol, Tokyo, pp 63–75

  • Rao RS, Kumar CG, Prakasham RS, Hobbs PJ (2008) The Taguchi methodology as a statistical tool for biotechnological applications: a critical appraisal. Biotechnol J 3:510–523

    Article  CAS  PubMed  Google Scholar 

  • Richards TA, Meredith DMJ, Guy L, David B (2012) Marine fungi: their ecology and molecular diversity. Annu Rev Mar Sci 4:495–522

    Article  Google Scholar 

  • Sahoo D, Tang XR, Yarish C (2002) Porphyra—the economic seaweed as a new experimental system. Current Sci 83:1313–1316

    Google Scholar 

  • Saito S, Sasaki M (1973) Studies on red rot disease of Porphyra. In: Japanese Society of Fisheries Science (ed) The disease of cultivated Porphyra. Koseisha Koseikaku, Tokyo, Japan, pp 59–69

  • Saleem M, Ali MS, Hussain S, Jabbar A, Ashraf M, Lee YS (2007) Marine natural products of fungal origin. Nat Prod Rep 24:1142–1152

    Article  CAS  PubMed  Google Scholar 

  • Simmons EG (1992) Alternaria taxonomy: current status, viewpoint, challenge. In: Chelkowski J, Visconti A (eds) Alternaria: biology, plant diseases and metabolites. Elsevier, Amsterdam, pp 1–35

    Google Scholar 

  • Smith JL, Summers G, Wong R (2010) Nutrient and heavy metal content of edible seaweeds in New Zealand. N Z J Crop Hort Sci 38:19–28

    Article  CAS  Google Scholar 

  • Takahashi M (1970) Identification of genus Pythium. Plant Prot 24:339–346

    Google Scholar 

  • Takahashi M, Ichitani T, Sasaki M (1977) Pythium porphyrae Takahashi et Sasaki, sp. nov. causing red rot of marine algae Porphyra spp. Trans Mycol Soc Jpn 18:279–285

    Google Scholar 

  • Takashi T, Yoshiaki H, Kazuya A, Kouhei O, Motoichiro K, Yasunori A, Mayumi E, Mikihiro Y, Hiroshi O (2013) Host-selective toxins produced by the plant pathogenic fungus Alternaria alternate. FEMS Microbiol Rev 37:44–66

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomma BPHJ (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker SL, Talbot NJ (2001) Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annu Rev Phytopathol 39:385–417

    Article  CAS  PubMed  Google Scholar 

  • Uppalapat S, Fujita Y (2000) Carbohydrate regulation of attachment, encystment, and appressorium formation by Pythium porphyrae (Oomycota) zoospores on Porphyra yezoensis (Rhodophyta). J Phycol 36:359–366

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 253–288

    Google Scholar 

  • Yu SH, Cho HS, Kim BR, Park MS (2003) Morphological and molecular characterization of Alternaria isolates from Solanaceous crops. Korean J Mycol 31:103–113

    Article  Google Scholar 

  • Zhang Y, Mu J, Feng Y, Kang Y, Zhang J (2009) Broad-spectrum antimicrobial epiphytic and endophytic fungi from marine organisms: isolation, bioassay and taxonomy. Mar Drugs 7:97–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng CJ, Shao CL, Guo ZY, Chen JF, Deng DS (2012) Bioactive hydroanthraquinones and anthraquinone dimers from a soft coral-derived Alternaria sp. fungus. J Nat Prod 75:189–197

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project was supported by the National High Technology Research and Development Program (2012AA10A406, 2012AA10A401, and 2012AA10A411), the National Natural Sciences Foundation of China (31372517), and the Special Independent Innovation Foundation of Shandong Province (2013CXC80202).

Author information

Authors and Affiliations

  1. Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, Shandong Province, China

    Shufen Li, Fanna Kong, Xianghai Tang & Yunxiang Mao

  2. Key Laboratory of Sustainable Development of Marine Fisheries, The Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, Shandong Province, China

    Zhaolan Mo

  3. National Laboratory for Marine Science and Technology, Qingdao, 266200, Shandong Province, China

    Zhaolan Mo & Yunxiang Mao

Authors
  1. Zhaolan Mo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shufen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fanna Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianghai Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yunxiang Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yunxiang Mao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mo, Z., Li, S., Kong, F. et al. Characterization of a novel fungal disease that infects the gametophyte of Pyropia yezoensis (Bangiales, Rhodophyta). J Appl Phycol 28, 395–404 (2016). https://doi.org/10.1007/s10811-015-0539-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-015-0539-z

Keywords

Search

Navigation