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Identification and Characterization of Pathogenic and Endophytic Fungal Species Associated with Pokkah Boeng Disease of Sugarcane

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Identification and Characterization of Pathogenic and Endophytic Fungal Species Associated with Pokkah Boeng Disease of Sugarcane Plant Pathol. J. 33(3) : 238-248 (2017) https://doi.org/10.5423/PPJ.OA.02.2017.0029 The Plant Pathology Journal pISSN 1598-2254 eISSN 2093-9280 ©The Korean Society of Plant Pathology Research Article Open Access Identification and Characterization of Pathogenic and Endophytic Fungal Species Associated with Pokkah Boeng Disease of Sugarcane Angelyn Hilton1, Huanming Zhang2, Wenying Yu3, and Won-Bo Shim1,2* 1Department of Plant Pathology & Microbiology, Texas A&M University, College Station, TX 77843-2132, USA 2Bioenvironmental Science, Texas A&M University, College Station, TX 77843-2132, USA 3College of Life Sciences, Fujian Agricultural and Forestry University, Fuzhou 350002, People’s Republic of China (Received on February 3, 2017; Revised on March 13, 2017; Accepted on March 20, 2017) Pokkah Boeng is a serious disease of sugarcane, which can lead to devastating yield losses in crop-producing Handling Associate Editor : Jeon, Junhyun regions, including southern China. However, there is still uncertainty about the causal agent of the disease. Our aim was to isolate and characterize the pathogen Sugarcane is an economically important crop worldwide through morphological, physiological, and molecular with many agricultural and industrial uses including ani- analyses. We isolated sugarcane-colonizing fungi in mal feed, sweeteners, biofuels, and bagasse. Sugarcane is Fujian, China. Isolated fungi were first assessed for produced in tropical and subtropical countries, including their cell wall degrading enzyme capabilities, and five southern regions of People’s Republic of China, which is isolates were identified for further analysis. Internal now the fourth largest producer of sugarcane worldwide transcribed spacer sequencing revealed that these five (Anderson-Sprecher and Wei, 2015; Koo and Taylor, strains are Fusarium, Alternaria, Phoma, Phomopsis, 2014). China produced over 126 million ton of sugarcane and Epicoccum. The Fusarium isolate was further in 2013, but due to recent profit losses, increasing produc- identified as F. verticillioides after Calmodulin and tion costs, unfavorable climatic events and disease pres- EF-1α gene sequencing and microscopic morphology sures, production levels are now decreasing up to 7% each study. Pathogenicity assay confirmed that F. verticil- year (Anderson-Sprecher and Wei, 2015; FAO, 2015). lioides was directly responsible for disease on sugar- Sugarcane is vulnerable to over 100 diseases, which can cane. Co-inoculation of F. verticillioides with other cause major declines in the annual yield of sugarcane isolated fungi did not lead to a significant difference in (Matsuoka and Maccheroni, 2015). Despite the produc- disease severity, refuting the idea that other cellulolyt- tion decline, the demand for sugarcane still outweighs the ic fungi can increase disease severity as an endophyte. annual yield making China the number one importer of This is the first report characterizing pathogenic F. sugarcane (Koo and Taylor, 2014). It is therefore critical verticillioides on sugarcane in southern China. to address the ongoing threats to the sugarcane industry in China and around the world. Keywords : cell-wall degrading enzymes, endophytic Pokkah Boeng is a re-emerging disease of sugarcane fungi, Fusarium verticillioides, Pokkah Boeng, sugarcane which has been found recently to cause major yield losses in most sugarcane producing regions, including South Af- rica, Malaysia, India, and China (Lin et al., 2014; McFar- *Corresponding author. lane and Rutherford, 2005; Sidique and Nordahliawate, Phone) +1-979-458-2190, FAX) +1-979-845-6483 2007; Singh et al., 2006; Vishwakarma et al., 2013). E-mail) [email protected] Pokkah Boeng disease was first described by Walker cc This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// and Went in 1896, and the name originates from a Java- creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non- nese for ‘malformed top’ (Martin et al., 1989). The usual commercial use, distribution, and reproduction in any medium, provided symptoms include red streaking, chlorosis, malformation, the original work is properly cited. and stalk rot. The disease is known to cause 10–38% Articles can be freely viewed online at www.ppjonline.org. Fungi Associated with Sugarcane Pokkah Boeng Disease 239 yield losses in the susceptible sugarcane variety POJ 2878 production was downregulated in LmSNF1 knockout (Ricaud et al., 2012). Research in India revealed overall mutants, and strains were avirulent with a reduction in fit- increase in disease incidence in all sugarcane varieties ness. Furthermore, Jorge et al. (2006) measured the pro- from 2007 to 2013, particularly up to 90% infection in duction of polygalacturonase, pectate lyase and xylanase variety S224/20 (Lin et al., 2014; Moretti, 2009). Histori- CWDEs by Fusarium oxysporum f. sp. ciceris during dis- cally, the incidence of Pokkah Boeng increase following ease development in chickpea. The production of CWDEs major rain events or post monsoon season. However, the was positively correlated to symptom development in disease is now present throughout the growing season leaves and stems, indicating that CWDEs are important during both wet and dry periods (Lin et al., 2014). for F. oxysporum f. sp. ciceris pathogenicity. Sugarcane is The causal agent of Pokkah Boeng is still ambiguous a row crop with high recalcitrant lignocellulosic content, and disputed amongst researchers. In older literature, therefore it would be reasonable to hypothesize that the Fusarium moniliforme is named as the causal pathogen. causal agent of Pokkah Boeng produces a high level of However, Fusarium classification and nomenclature sys- cellulolytic CWDE during plant pathogenesis. tem has gone through its turbulent transformation, and The aim of this study was to isolate and characterize researchers have not been able to come to a consensus on the causal agent of Pokkah Boeng through morphologi- which Fusarium species is the appropriate forma specialis cal, physiological, and molecular genetic analyses. We (f. sp.) for Pokkah Boeng pathogen. Recent studies have isolated the fungal strains from diseased crops sampled suggested F. sacchari, F. fujikuroi, F. verticillioides, F. from a sugarcane breeding research field in Fujian, China. andiyazi, and F. proliferatum as the causal agents (Lin et Isolates were assessed for the production of cellulase, a al., 2014; McFarlane and Rutherford, 2005; Sidique and prominent CWDE. In addition, the isolates were inocu- Nordahliawate, 2007; Singh et al., 2006; Vishwakarma et lated into sugarcane stalks to assess for pathogenicity. al., 2013). This is in part due to the ambiguity of Fusar- Co-inoculations were also performed to gain an under- ium taxonomy particularly in the Liseola section, which standing of microbial interactions in situ. We performed includes F. verticillioides, F. proliferatum and F. fujikuroi molecular analyses of the isolated strains to determine (Leslie and Summerell, 2011). Gibberella fujikuroi, or the identity of Pokkah Boeng causal agent. Our goal was section Liseola, includes eight known mating populations, to gain a better understanding of this critical disease and which are capable of causing disease on a wide range of how the pathogen is able to produce such devastating out- crops such as maize, sugarcane, and sorghum (Bandyo- comes on sugarcane crops. padhyay et al., 2008; Kerényi et al., 1999; Zakaria et al., 2011). These species are also known to produce a variety Materials and Methods of mycotoxins that are detrimental to human and animal health, making the study of these pathogens economically Field sampling. Diseased sugarcane samples were col- and socially significant. The classification of species fall- lected in the Sugarcane Breeding Research Field at the ing under section Liseola has gone through both expan- Fujian Agriculture and Forestry University (FAFU) in sion and contraction since the first description of Fusar- China. The area of the FAFU sugarcane research field ium by Wollenweber and Reinking in 1935 (Waalwijk et (approximately 7 hectares) was separated into two al., 1996; Wollenweber and Reinking, 1935). With current 3.5-hectare sections, and one of the sections was cho- ambiguity surrounding the causal agent of Pokkah Boeng, sen for sampling. The sugarcane cultivar grown in the one of the important needs is to characterize the etiology 3.5-hectare field is ROC22, a hybrid of Saccharum of- of pathogenic Fusarium species in sugarcane. ficinarum and Saccharum spontaneum. The sampled area In terms of virulence, we still have a limited under- was further divided into four different quadrants and an standing of how Fusarium pathogens cause disease in equal number of diseased plants were randomly taken sugarcane. When we consider rot diseases in crops, it is from each quadrant. Diseased plants were observed for reasonable to anticipate that fungal enzymes play a sig- the following symptoms: leaf malformation, leaf curling, nificant role. Many plant pathogenic fungi require cell stalk rot, red streaking, and necrosis. Samples were cut, wall degrading enzymes (CWDE) for successful invasion placed in plastic bags and labeled before returning to the of plant cell walls and ultimately cause disease (Kubicek lab for surface sterilization. A total of 74 diseased plants et al., 2014). For example, a pectate lyase gene PL1332 were sampled in June of 2014. Images of the sampled in Alternaria brassicicola
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