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For Review Only Songklanakarin Journal of Science and Technology SJST-2017-0350.R2 MOHKTAR Histological description of Exobasidium vexans infection on tea leaves (Camellia sinensis) Journal: Songklanakarin Journal of Science and Technology ManuscriptFor ID SJST-2017-0350.R2 Review Only Manuscript Type: Original Article Date Submitted by the Author: 26-May-2018 Complete List of Authors: MOHKTAR, NORSYUHADA; SCHOOL OF BIOLOGICAL SCIENCES; Nagao, Hideyuki; Universiti Sains Malaysia, School of Biological Sciences Keyword: leaf gall, cell differentiation, mesophyll, phloem, disease severity For Proof Read only Page 1 of 23 Songklanakarin Journal of Science and Technology SJST-2017-0350.R2 MOHKTAR 1 2 3 Original Article 4 5 Exobasidium vexans 6 Histological description of infection on tea leaves 7 8 (Camellia sinensis) 9 10 Norsyuhada Mohktar1, Hideyuki Nagao1 11 12 1School of Biological Sciences, Universiti Sains Malaysia, Pulau Pinang, 11800, Malaysia 13 14 15 * Corresponding author, Email address: [email protected] 16 17 18 19 For Review Only 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 For Proof Read only Songklanakarin Journal of Science and Technology SJST-2017-0350.R2 MOHKTAR Page 2 of 23 1 2 3 4 5 1 Abstract 6 7 8 2 Exobasidium vexans Massee is a parasitic fungus that causes tea blister blight. Tea blister blight 9 10 3 is characterised by the swelling of the infected spots on the tea leaves. To date, there is limited 11 12 4 information on the cellular alterations that occur during E. vexans infection. The aim of this 13 14 5 study was to observe the histological changes on tea leaves infected by E. vexans. Diseased and 15 16 17 6 healthy leaves were thin-sliced by cryostat microtome and examined by light microscopy. 18 19 7 Observations on the thin Forsections revealedReview the mode ofOnly hymenium development in E. vexans in 20 21 8 which the basidia protruded between the epidermal cells. The infection caused hypertrophy as 22 23 24 9 the size of the cells at the infected spots became double the size of the healthy cells. The first 25 26 10 description of venous infections of E. vexans were also described. The proliferation of the fungus 27 28 11 on the vein resulted in the formation of hymenium on both lower and upper sides of the leaves 29 30 31 12 and there was complete disruption of the vascular bundle in the leaves vein. Blister blight disease 32 33 13 on the tea plantation in this study was found to be moderately severe. Morphological and 34 35 14 molecular identification confirmed that the fungus isolated from the symptomatic leaves was E. 36 37 15 vexans. 38 39 40 16 Keywords: Disease severity, leaf galls, cell differentiation, mesophyll, phloem, plant parasite 41 42 43 44 17 1. Introduction 45 46 18 Tea has been one of the most consumed drinks in the world. The drink originates from 47 48 49 19 the leaves of tea plants (Camellia sinensis (L.) Kuntze) that are processed and dried for brewing. 50 51 20 Exobasidium vexans Massee is a pathogenic plant fungus that infects tea plants and causes tea 52 53 21 blister blight. The spread of this disease has brought tremendous loss to tea production industry 54 55 56 22 and it has become a serious threat to all tea plantations across Asia including India, Sri Lanka, 57 58 59 60 For Proof Read only Page 3 of 23 Songklanakarin Journal of Science and Technology SJST-2017-0350.R2 MOHKTAR 1 2 3 23 Japan and Indonesia (Baby, 2002). As the number one tea producer to the global market, India 4 5 6 24 has about 5 million hectares of land dedicated to tea plantation (Boriah, 2002). The country 7 8 25 which had contributed up to 23% of total world tea production suffered a great loss due to tea 9 10 26 blister blight as the pathogen attacks harvestable young shoots resulting in up to 40% yield losses 11 12 27 (Gulati, Gulati, Ravindranath, & Chakrabarty, 1993; Basu, Bera, & Rajan, 2010). In addition, 13 14 15 28 tea blister blight has inflicted a severe crop loss in Sri Lanka in which 33% of yield reduction 16 17 29 was recorded in unprotected areas compared to fields which were sprayed with chemicals (de 18 19 30 Silva, Murugiah, & Saravapavan,For Review 1997). Transgenic Only tea plant that is resistant to E. vexans 20 21 22 31 infection has been developed in which the clone expresses higher amount of chitinase enzyme to 23 24 32 hydrolyse the cell wall of the invading fungus (Jeyaramraja, Pius, Manian, & Nithya Meenakshi, 25 26 33 2005; Jayaswall, Mahajan, Singh, Parmar, Seth et al., 2016). 27 28 29 34 Symptoms of E. vexans infection include the swelling and formation of conspicuous 30 31 35 white hymenium on the infected spots that will eventually necrotise. Several studies have been 32 33 36 done on the histology of plants infected by other Exobasidium species. According to Mims and 34 35 37 Richardson (2007) and Lee, Lee, Shin, Park, and Sieber (2015), the infection of Exobasidium 36 37 38 38 gracile (Shirai) Syd, and P. Syd on Camellia sasanqua Thunb. was characterised by the 39 40 39 formation of a distinct pseudoparenchymatous layer of intercellular hyphae which initially 41 42 40 developed several layers above the lower epidermis. Eventually the lower epidermis layer 43 44 45 41 became sloughed off to give rise to the white hymenium on the underside of the leaf (Mims & 46 47 42 Richardson, 2007; Lee et al., 2015). Meanwhile, Li and Guo (2008) described a different mode 48 49 43 of hymenium development in the infection caused by Exobasidium ovalifoliae Z. Y. Li and L. 50 51 52 44 Guo in which the basidia protruded between epidermal cells to form continuous white hymenium 53 54 45 upon reaching the final stage of infection. Gadd and Loos (1949) reported that the formation of 55 56 57 58 59 60 For Proof Read only Songklanakarin Journal of Science and Technology SJST-2017-0350.R2 MOHKTAR Page 4 of 23 1 2 3 46 hymenium in E. vexans progressed in the similar manner but they only provided an illustration to 4 5 6 47 support their observation. 7 8 48 At the cellular level, the enlargement of the infected spots caused by the infection of 9 10 49 Exobasidium species is either due to hypertrophy or hyperplasia – an increase in the number of 11 12 50 the cells. For example, Graafland (1960) reported that both hypertrophy and hyperplasia 13 14 15 51 occurred in the infection of Exobasidium japonicum Shirai on the leaves of Azaleas. Meanwhile, 16 17 52 the flowers of Lyonia ferruginea (Walter) Nutt. that were infected with Exobasidium ferrugineae 18 19 53 Minnis, A.H. Kennedy &For N.A. Goldberg Review only became Only hypertrophied but this observation was 20 21 22 54 less common in the leaves of the plant (Kennedy, Goldberg, & Minnis, 2012). 23 24 55 Several methods have been developed to measure the severity of fungal diseases on tea 25 26 56 plants. Webster and Park (1956) first evaluated the severity of E. vexans infection based on the 27 28 29 57 disease incidence from a pool of sampled leaves. Meanwhile Balasuriya (2003) assessed blister 30 31 58 blight infection according to the number of blistered lesion on tea leaves. Recently, Sinniah, 32 33 59 Wasantha Kumara, Karunajeewa and Ranatunga (2016) developed an improvised assessment 34 35 60 key to evaluate the severity of E. vexans infection on tea leaves that accounted for both host 36 37 38 61 reactions and the sequential stages of symptom development. 39 40 62 To date, there have been no detailed descriptions on the histological aspects of E. vexans 41 42 63 infection on C. sinensis except the illustration provided by Gadd and Loos (1949). Hence, the 43 44 45 64 aim of this study is to provide a deeper understanding on the histological changes that occurred 46 47 65 to C. sinensis leaf cells upon E. vexans infection. The mode of hymenium development and the 48 49 66 effect of E. vexans infection on the architectural state of the leaf cells were examined. In 50 51 52 67 addition, microscopic descriptions of venous infection were also presented. Disease severity of 53 54 68 E. vexans infection on the tea plantation in this study was assessed and the morphology of 55 56 57 58 59 60 For Proof Read only Page 5 of 23 Songklanakarin Journal of Science and Technology SJST-2017-0350.R2 MOHKTAR 1 2 3 69 basidia and basidiospores of this fungus was described. Finally, a phylogenetic tree was 4 5 6 70 constructed based on the internal transcribed spacer (ITS) gene to assess the position of E. 7 8 71 vexans relative to other Exobasidium species. 9 10 11 12 72 2. Materials and Methods 13 14 2.1 Histology of E. vexans infection 15 73 16 17 18 74 Healthy and infected shoots of tea leaves were collected from MARDI Agro-technology 19 For Review Only 20 75 Park, Cameron Highlands, Malaysia in August 2016 and preserved in formalin acetic acid 21 22 76 solution. The vein and lamina of both healthy and infected spots were bounded to specimen 23 24 blocks by Jung Tissue Freezing Medium® (Leica Microsystems, Nussloch, Germany). The 25 77 26 27 78 samples were then transversely thin-sliced by cryostat microtome (-20°C) at 10µm thickness 28 29 79 (Leica CM 1850 UV, Nussloch, Germany).
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