Sains Malaysiana 48(8)(2019): 1609–1618

http://dx.doi.org/10.17576/jsm-2019-4808-06

Distribution, Diversity, and Specificity of a Parasitic Algal Genus Cephaleuros in Thailand

(Taburan, Kepelbagaian dan Kekhususan dalam Genus Alga parasit Cephaleuros di Thailand)

WIKROM CHANTHAPATCHOT & ANCHITTHA SATJARAK*

Department of Botany, Chulalongkorn University, Bangkok, 10330, Thailand  

Received: 8 March 2019/Accepted: 12 May 2019

ABSTRACT

Cephaleuros has been recognized as a terrestrial parasitic green algal genus causing algal red rust diseases which have violently damaged economic crops worldwide. To obtain information of the algal distribution in Thailand and to understand the specificity of the algal parasite and their hosts, we reviewed the reports on this algal genus in Thailand and performed comparative analyses of the algal-host specificity. Results indicated that more than 10 species of Cephaleuros have been reported across Thailand. Their presence varies from regions to regions with the highest numbers of reports from the southern part of Thailand. The leaf area of infection also varied due to the different algal infecting mechanisms. We found that C. annonae, C. drouetii, C. henningsii, C. lagerheimii, C. parasiticus, C. pilosa, C. piperis and C. solutus appeared to be specific to plant family while C. diffusus, C. expansa, C. karstenii, C. tumidae-setae and C. virescens infected wider range of plant species. Among these, C. virescens had the highest number of reports as it was present in all the regions of Thailand where it infected various plant species belonging to more than 20 plant families. Analyses of C. virescens suggested the presence of putative sequence of gene encoding a virulence protein in this alga. The information on the distribution and algal-host specificity might help in understanding the spread of this red rust plant disease due to the algal genus Cephaleuros in Thai economic plants.

Keywords: Algal red rust disease; Cephaleuros; green algae; parasitic algae; specificity

ABSTRAK

Cephaleuros telah diiktiraf sebagai genus alga hijau parasit daratan yang menyebabkan penyakit karat merah alga yang telah merosakkan tanaman ekonomi di seluruh dunia. Untuk mendapatkan maklumat tentang sebaran alga ini di Thailand dan untuk memahami kekhususan parasit alga dan hos, kami mengkaji laporan mengenai genus alga ini di Thailand dan melakukan analisis komparatif tentang kekhususan algal-hos. Hasil kajian menunjukkan bahawa lebih daripada 10 spesies Cephaleuros telah dilaporkan di seluruh Thailand. Kehadiran spesies tersebut berbeza di kawasan berbeza dengan bilangan tertinggi laporan dari bahagian selatan Thailand. Kawasan jangkitan daun juga berubah disebabkan oleh mekanisme jangkitan alga yang berbeza. Kami mendapati C. annonae, C. drouetii, C. henningsii, C. lagerheimii, C. parasiticus, C. pilosa, C. piperis dan C. solutus didapati khusus untuk famili tumbuhan tertentu manakala C. diffusus, C. expansa, C. karstenii, C. tumidae-setae dan C. virescens menjangkiti pelbagai spesies tumbuhan. Antaranya, C. virescens mempunyai bilangan laporan tertinggi yang terdapat di semua wilayah Thailand dan menjangkiti pelbagai spesies tumbuhan melebihi daripada 20 famili tumbuhan. Analisis C. virescens mencadangkan kehadiran jujukan gen putatif yang mengekodkan protein kevirulenan dalam alga ini. Maklumat tentang sebaran dan kekhususan alga-hos mungkin membantu dalam memahami penyebaran penyakit tumbuhan karat merah yang disebabkan oleh genus Cephaleuros dalam tumbuhan ekonomi Thai.

Kata kunci: Alga hijau; alga parasit; Cephaleuros; kekhususan; penyakit karat merah alga

REFERENCES

Athipanyākhom, P., Sī madư̄a, S., Dūangsaʻāt, C., Khōsit čharoēnkun, N., Tangčhit somkid, N. & Tantiwānit, Y. 2011. Diseases survey and diagnosis for exported plant diseases survey and diagnosis for exported plant s for exported plant: Papaya and aromatic coconut, imported plant: Oil palm and ornamental bulb (Research report). Bangkok: Department of Agriculture.

Athipanyākhom, P., Likhitʻēkkarāt, S. & Trakūnsukrat, P. 2010. Study on jujube diseases for imported plants. (Research report). Bangkok: Department of Agriculture.

Brooks, F.E. 2004. Plant-parasitic algae (Chlorophyta: Trentepohliales) in American Samoa. Pacific Science 58(3): 419-428.

Bunjongsiri, P. & Sunpapao, A. 2018. Optimal growth conditions for in vitro cultures of plant parasitic algae Cephaleuros Kunze ex E. M. fries. Philippine Agricultural Scientist 101: 45-50.

Bunjongsiri, P., Pitaloka, M.K. & Sunpapao, A. 2016. Isolation, identification and morphological features of plant parasitic algae in genus Cephaleuros spp. on synthetic media. Khon Kaen Agriculture Journal 44(1): 918-923.

Bunjongsiri, P., Thithuan, N., Phoka, N., Arikit, S. & Sunpapao, A. 2016. Green algae order Trentepohliales (Chlorophyta, Ulvophyceae) and impact on longkong host (Lansium domesticum Corr.). Songklanakarin Journal of Plant Science 3(1): M09/24-30.

Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K. & Madden, T. 2009. BLAST+: Architecture and applications. BMC Bioinformatics 10: 421-430.

Chapman, R.L. & Good, B.H. 1983. Subaerial symbiotic green algae: Interactions with vascular plant hosts. In Algal Symbiosis: A Continuum of Interaction Strategies, edited by Goff, L.J. Cambridge, UK: Cambridge University Press. pp. 173-204.

Guiry, M.D. & Guiry, G.M. 2019. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed on February 22, 2019.

Hadwiger, L.A. 2008. Pea-Fusarium solani interactions contributions of a system toward understanding disease resistance. Phytopathology 98(4): 372-379.

Holcomb, G.E. 1986. Hosts of the parasitic alga Cephaleuros virescens in Louisiana and new host records for the continental United States. Plant Disease 70: 1080-1083.

Jiang, R.H.Y., Tripathy, S., Govers, F. & Tyler, B.M. 2008. RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proceedings of the National Academy of Sciences 105(12): 4874-4879.

Jose, G. & Chowdary, Y.B.K. 1980. Studies on the host range of the endophytic alga Cephaleuros Kunze in India. Revista de Biología Tropical 28: 297-304.

Joubert, J.J. & Rijkenberg, F.H.J. 1971. Parasitic green algae. Annual Review of Phytopathology 9: 45-64.

López-bautista, J.M., Rindi, F. & Guiry, M.D. 2006. Molecular systematics of the subaerial green algal order Trentepohliales: An assessment based on morphological and molecular data. International Journal of Systematic and Evolutionary Microbiology 56: 1709-1715.

Lopez-Bautista, J.M., Waters, D.A. & Chapman, R.L. 2002. The Trentepohliales revisited. 83.1. http://ucjeps.berkeley.edu/ constancea/83/lopez_etal/trentepohliales.html.

Marlatt, R.B. & Alfieri, S.A. 1981. Hosts of a parasitic alga, Cephaleuros Kunze, in Florida. Plant Disease 65: 520-522.

Matasci, N., Hung, L.H., Yan, Z., Carpenter, E.J., Wickett, N.J., Mirarab, S., Nguyen, N., Warnow, T., Ayyampalayam, S., Barker, M., Burleigh, J.G., Gitzendanner, M.A., Wafula, E., Der, J.P., dePamphilis, C.W., Roure, B., Philippe, H., Ruhfel, B.R., Miles, N.W., Graham, S.W., Mathews, S., Surek, B., Melkonian, M., Soltis, D.E., Soltis, P.S., Rothfels, C., Pokorny, L., Shaw, J.A., DeGironimo, L., Stevenson, D.W., Villarreal, J.C., Chen, T., Kutchan, T.M., Rolf, M., Baucom, R.S., Deyholos, M.K., Samudrala, R., Tian, Z., Wu, X., Sun, X., Zhang, Y., Wang, J., Leebens-Mack, J. & Wong, G.K. 2014. Data access for the 1,000 plants (1KP) project. GigaScience 3: 17.

Morgan, W. & Kamoun, S. 2007. RXLR effectors of plant pathogenic oomycetes. Current Opinion in Microbiology 10(4): 332-338.

Muthukumar, T., Uma, E. & Perumalsamy, P. 2014. Occurrence of foliicolous parasitic alga Cephaleuros virescens on cultivated ornamental plants in southern India. Botanica Lithuanica 20: 87-98.

Nelson, S.C. 2008. Cephaleuros species, the plant-parasitic green algae. Plant Disease 43: 1-7.

Osuna-Cruz, C.M., Paytuvi-Gallart, A., Di Donato, A., Sundesha, V., Andolfo, G., Cigliano, R.A., Sanseverino, W. & Ercolano, M.R. 2017. PRGdb 3.0: A comprehensive platform for prediction and analysis of plant disease resistance genes. Nucleic Acids Research 46(D1): D1197-D1201.

Pitaloka, M.K., Petcharat, V. & Sunpapao, A. 2014. Cephaleuros solutus Karsten, as a causal agent of durian (Durio zibethinus Murray) algal leaf spot disease in Thailand. Khon Kaen Agriculture Journal 42(3): 644-648.

Pitaloka, M.K., Petcharat, V., Arikit, S. & Sunpapao, A. 2015. Cephaleuros virescens, the cause of an algal leaf spot on Para rubber in Thailand. Australasian Plant Disease Notes 10: 1-4.

Pongpanich, K. 1997. Diseases of Acacia species in Thailand. In Diseases of Tropical Acacias: Proceedings of an International Workshop, Subanjeriji (South Sumatra) 28: 62-69.

Pornsuriya, C., Sunpapao, A., Srihanant, N., Worapattamasri, K., Kittimorakul, J., Phithakkit, S. & Petcharat, V. 2013. A survey of diseases and disorders in oil palms of Southern Thailand. Plant Pathology Journal 12(4): 169-175.

Raffaele, S. & Kamoun, S. 2012. Genome evolution in filamentous plant pathogens: Why bigger can be better. Nature Reviews Microbiology 10(6): 417-430.

Ratanapaiboonkit, K. & Brocklehurst, T. 2016. Isolation and pigment investigation of plant pathogenic algae genus Cephalueros. KMUTT Research and Development Journal 38(4): 367-382.

Sanyong, S. & Amarakul, V. 2001. GIS application for plant diseases distribution on jack fruit, bael fruit, ma kiang trees in lower northern part of Thailand. In Proceedings of the 22nd Asian Conference on Remote Sensing. Centre for Remote Imaging, Sensing and Processing (CRISP). Singapore Institute of Surveyors and Valuers (SISV), and Asian Association of Remote Sensing (AARS), Singapore.

Schulte, M.J., Martin, K. & Sauerborn, J. 2007. Efficacy of spiromesifen on Aceria litchii (Keifer) in relation to Cephaleuros virescens Kunze colonization on leaves of litchi (Litchi chinensis Sonn.). Journal of Plant Diseases and Protection 114(3): 133-137.

Sunpapao, A. 2016. Parasitism of green algae Cephaleuros Kunze ex E.M. Fries. Khon Kaen Agriculture Journal 44(1): 905-910.

Sunpapao, A. 2016. Plant Parasitic Algae. Bangkok: Kasetsart University.

Sunpapao, A. & Pitaloka, M.K. 2017. Two new species of Cephaleuros (Chlorophyta, Ulvophyceae) from Southern Thailand. Phykos 47(2): 5-9.

Sunpapao, A. & Pitaloka, M.K. 2015. A new record of plant parasitic green algae, Cephaleuros diffusus (Trentepohliaceae, Chlorophyta), on Acacia auriculiformis hosts in Thailand. Biodiversitas Journal of Biological Diversity 16(2): 116-120.

Sunpapao, A., Bunjongsiri, P., Thithuan, N. & Arikit, S. 2017. First report of Cephaleuros virescens causing algal leaf spot of Manilkara zapota in Thailand. Plant Disease 101(4): 636.

Sunpapao, A., Pitaloka, M.K. & Arikit, S. 2016. Algal leaf spot associated with Cephaleuros virescens (Trentepohliales, Ulvophyceae) on Nephelium lappaceum in Thailand. Biodiversitas Journal of Biological Diversity 17(1): 31-35.

Sunpapao, A., Thithuan, N., Bunjongsiri, P. & Arikit, S. 2016. Cephaleuros parasiticus, associated with algal spot disease on Psidium guajava in Thailand. Australasian Plant Disease Notes 11(1): 12.

Sunpapao, A., Thithuan, N., Pitaloka, M.K. & Arikit, S. 2016. Algal leaf spot of Lansium parasiticum caused by Cephaleuros sp. in Thailand. Journal of Plant Pathology 98(2): 369-377.

Sunpapao, A., Pitaloka, M.K. & Arikit, S. 2015. The genus Cephaleuros Kunze ex EM Fries (Trentepohliales, Ulvophyceae) from Southern Thailand. Nova Hedwigia 101(3): 451-462.

Sunpapao, A., Pitaloka, M.K. & Petcharat, V. 2015. Host range, distribution and diversity of plant parasitic algae Cephaleuros Kunze in Southern Thailand. Khon Kaen Agriculture Journal 43(1): 928-932.

Sunpapao, A., Pitaloka, M.K., Thithuan, N., Tantipalanon, O. & Petcharat, V. 2015. Morphology and disease severity of plant parasitic algae Cephaleuros Kunze. Khon Kaen Agriculture Journal 43(1): 189-194.

Suto, Y. & Ohtani, S. 2011. Morphological features and chromosome numbers in culture of five Cephaleuros species (Trentepohliaceae, Chlorophyta) from Japan. Phycological Research 59: 42-51.

Suto, Y. & Ohtani, S. 2009. Morphology and taxonomy of five Cephaleuros species (Trentepohliaceae, Chlorophyta) from Japan, including three new species. Phycologia 48: 213-236.

Suto, S., Ganesan, E.K. & West, J.A. 2014. Comparative observations on Cephaleuros parasiticus and C. virescens (Trentepohliaceae, Chlorophyta) from India. Algae 29: 121-126.

Thithuan, N. & Sunpapao, A. 2016. Cephaleuros virescens complex cause algal spot disease on Michelia alba and Magnolia sirindhorniae. Khon Kaen Agriculture Journal 44(1): 911-917.

Thithuan, N., Bunjongsiri, P., Phoka, N., Arikit, S. & Sunpapao, A. 2016. Development of reproductive structures of plant parasitic algae Cephaleuros Kunze ex E.M. Fries on longkong (Lansium domesticum Corr.). Songklanakarin Journal of Plant Science 3(1): 31-35.

Thompson, R.H. & Wujek, D.E. 1997. Trentepohliales, Cephaleuros, Phycopeltis and Stomatochroon: Morphology, Taxonomy and Ecology. 1st ed. Enfield, N.H.: Science Publishers.

Thompson, R.H. & Wujek, D.E. 1992. Printzina gen. nov. (Trentepohliaceae), including a description of a new species. Journal of Phycology 28: 232-237.

Tyler, B.M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R.H.Y., Aerts, A., Arredondo, F.D., Baxter, L., Bensasson, D., Beynon, J.L., Chapman, J., Damasceno, C.M.B., Dorrance, A.E., Dou, D., Dickerman, A.W., Dubchak, I.L., Garbelotto, M., Gijzen, M., Gordon, S.G., Govers, F., Grunwald, N.J., Huang, W., Ivors, K.L., Jones, R.W., Kamoun, S., Krampis, K., Lamour, K.H., Lee, M.K., McDonald, W.H., Medina, M., Meijer, H.J.G., Nordberg, E.K., Maclean, D.J., Ospina- Giraldo, M.D., Morris, P.F., Phuntumart, V., Putnam, NH., Rash, S., Rose, J.K.C., Sakihama, Y., Salamov, A.A., Savidor, A., Scheuring, C.F., Smith, B.M., Sobral1, B.W.S., Terry, A., Torto-Alalibo, T.A., Win, J., Xu, Z., Zhang, H., Grigoriev, I.V., Rokhsar, D.S. & Boore, J.L. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261-1266.

Wisantanon, N. 2010. Handbook of Plant Disease Diagnosis Caused by Fungi and Algae and the Suggestion for Disease Control. Bangkok: Kasetsart University.

Wolf, F.A. 1930. A parasitic alga, Cephaleuros virescens Kunze, on citrus and certain other plants. Journal of Elisha Mitchell Scientific Society 45: 187-205.

Wonglom, P., Thithuan, N., Bunjongsiri, P. & Sunpapao, A. 2018. Plant-parasitic algae (Cephaleuros spp.) in Thailand, including four new records. Pacific Science 72(3): 363-372.

*Corresponding author; email: anchittha.satjarak@gmail.com