FIRST REPORTS ON FUNGAL PATHOGENS OF IMPROVED JUJUBE IN BANGLADESH

Authors: M. Z. Hoque1, M. A. Mannan Akanda2, I. H. Mian2 and M. K. A. Bhuiyan2

Abstract

Z. Hoque, M. A. Mannan Akanda, I. H. Mian and M. K. A. Bhuiyan. 2012. First reports on fungal pathogens of improved jujube in Bangladesh. Bangladesh J. Plant Pathol. 28(1&2):5-12.

A survey was conducted in Bangladesh to identify the fungal diseases of jujube (Ziziphus mauritiana Lam.) and their causal pathogens occur in commercial orchards, planted with high yield varieties. The identified diseases and their causal fungi were leaf spots (Alternaria alternata, Cercospora ziziphi, Curvularia lunata, Fusarium semitectum,  Lasiodiplodia theobromae, Mitteriella ziziphina, Pestalotiopsis palmarum), fruit spots and pre-harvest fruit rot (A. alternata,  Colletotrichum gloeosporioides, C. lunata, F. semitectum, L. theobromae, M. ziziphina, Nigrospora oryzae, P. palmarum, Phomopsis sp.), post-harvest fruit rot (A. alternata, Aspergillus spp., C. gloeosporioides, C. lunata, F. semitectum, Nigrospora oryzae, Penicillium spp., Phomopsis sp. P. palmarum, Rhizopus sp.), powdery mildew (Oidium erysiphoidess f. sp. ziziphi), sooty mould or black mold or Isariopsis mold (Isariopsis indica var. ziziphi, Capnodium sp.) and stem bleeding or gummosis (P. palmarum, C. lunata). Among the fungal pathogens causing jujube diseases, P. palmarum, C. gloeosporioides, A. alternata, F. semitectum, C. lunata, L. theobromae, C. ziziphi, Phomopsis sp., I. indica var. ziziphi, M. ziziphina and N. oryzae were noted as new records in Bangladesh.

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INTRODUCTION

Jujube (Ziziphus mauritiana Lam.) is a nutritious indigenous fruit of Bangladesh cultivated in homestead since time immemorial. The fruits contain high protein, phosphorus, calcium, carotene and vitamins (Kuliev and Guseinova 1974). Available reports from China and India reveal that jujube is vulnerable to many diseases (Singh and Singh 1979, Rai et al. 1982, Sharma et al. 1993, Nallathambi et al. 1999, Quin and Tian 2004). Alternaria alternata causes pre-harvest infection on jujube fruits that result in 25% yield loss in India (Nallathambi 1999, 2001). Moreover, jujube fruits are highly vulnerable to post-harvest color fading, browning, decay, and water loss. Powdery mildew caused by Oidium erysiphoides f.sp. ziziphi is a major disease of jujube  in India. Jamadar et al. (2009) found 50-60% loss in fruit yield due to powdery mildew of jujube and reduced market value of the produce. Pseudocercospora jujubae a fungal pathogen has been reported from Bangladesh by Khan et al.  (1983).

In Bangladesh, many diseases appear on foliage and fruits of jujube. In many cases, disease occurrence is  an  important  threat  for commercial cultivation of jujube. However, reports on the occurrence of diseases in Bangladesh are scanty (Rahman et al. 2011). Considering the above facts a study was undertaken to survey the occurrence of fungal diseases of jujube and their causal fungi in Bangladesh.

 

MATERIALS AND METHODS

Commercial jujube orchards were selected in five jujube growing districts of Bangladesh namely Gazipur, Pabna, Rajshahi, Rangpur and Mymensingh. The orchards were planted with three improved jujube varieties viz. apple Kul, BAU Kul and BARI Kul-1. A total of 405 diseased samples representing 150 fruits, 135 leaves, 30 trunks and 90 inflorescences of jujube were collected from the selected areas during 2007-08, 2008-09 and 2009-10. Among 150 fruit samples 73 were collected from markets of those locations. The collected samples were examined carefully and symptoms of individual diseases were recorded and photographs were taken.

Fungal pathogens associated with the diseased samples were isolated from infected plant samples following standard tissue planting methods using potato dextrose agar (PDA) medium as described by Aneza (2003). Whenever necessary, infected samples were placed in moist chambers and incubate at room (25 ±2 C) temperature for two days. Fungal mycelia grew from the samples were transferred directly to PDA plates.

Fungi isolated from the collected diseased specimens were purified following single spore culture and/or hyphal tip culture method (Aneza 2003). The isolated fungi were identified based on colony and morphological characters on PDA and consulting available literature (Barnett and Hunter 1972, Sutton 1980). Pathogenicity of different fungal pathogens isolated from diseased samples of jujube was performed following detached leaf and detached fruit inoculation method (Omar and Wahid 2001)

RESULTS AND DISCUSSION

Occurrence of diseases in Bangladesh

In Bangladesh, at least seven diseases were found to attack jujube in commercial orchard planted with high yielding varieties. These were leaf spots (Alternaria alternata, Cercospora ziziphi, Curvularia lunata, Fusarium semitectum,  Lasiodiplodia theobromae, Mitteriella ziziphina, Pestalotiopsis palmarum), fruit spots and pre-harvest fruit rot (A. alternata, Colletotrichum gloeosporioides, C. lunata, F. semitectum, L. theobromae, M. ziziphina, Nigrospora oryzae, P. palmarum, Phomopsis sp.), post-harvest fruit rot (A. alternata, Aspergillus spp. C. gloeosporioides, C. lunata,., F. semitectum, Nigrospora oryzae, Penicillium spp., Phomopsis sp. P. palmarum, Rhizopus sp.), powdery mildew (Oidium erysiphoidess f. sp. ziziphi), sooty mould or black mold or Isariopsis mold (Isariopsis indica var. ziziphi,Capnodium sp.) and stem bleeding or gummosis (P. palmarum, C. lunata). Harvested jujube fruits were found to be attacked by A. alternata, Aspergillus spp., C. gloeosporioides, C. lunata, F. semitectum, L. theobromae, Nigrospora sp., Penicillium spp., Phomopsis sp., P. palmarum, Rhizopus sp. causing post harvest fruit rot (Table 1).

Table 1. Diseases of jujube occur in Bangladesh and their causal fungi recorded during 2008 to 2010 crop seasons

Diseases Pathogens
Powdery mildew Oidium erysiphoidess f.sp ziziphi
Leaf spots Alternaria alternata, Cercospora ziziphi, Curvularia lunata, Fusarium semitectum,  Lasiodiplodia theobromae, Mitteriella ziziphina, Pestalotiopsis palmarum
Sooty, black or Isariopsis mold Isariopsis indica var. ziziphi, Capnodium sp.
Rust disease Phakopsora zizyphi-vulgaris
Stem bleeding or gummosis P. palmarum, F. semitectum, C. lunata
Fruit spots and Pre-harvest fruit rot A.,  Colletotrichum gloeosporioides, C. lunata, F. semitectum, L. theobromae, M. ziziphina, Nigrospora oryae, P. palmarum, Phomopsis sp.
Post-harvest fruit rot A. alternata, Aspergillus spp., C. gloeosporioides, C. lunata, F. semitectum, L. theobromae, F. semitectum , N. oryzae, Penicillium spp., Phomopsis sp. P. palmarum, Rhizopus sp.

Altogether 16 fungal pathogens were associated with diseased samples of jujube plants during the study. Of them, association of 11 fungi with jujube is new records in Bangladesh. They are A. alternata, C. ziziphi, C. gloeosporioides, C. lunata, F. semitectum, I. indica var. ziziphi, L. theobromae, M. ziziphina, Nigrospora sp., P. palmarum and Phomopsis sp. Results of their pathogenicity test on inoculated leaves and fruits, and their prevalence in collected samples are described below:

Alternaria alternata: Among the tested samples, one hundred eighty five samples yielded A. alternata. Characteristic muriform spores in chain were observed on culture plate as well as on infected plant parts (Plate I A & B). The pathogen causes leaf spot (Plate I C), fruit spot (Plate I D & E) and fruit rot (Plate I F). Symptoms of leaf spots are observed on the upper surface of leaves as small irregular, brown lesions. Dark brown to black spots are found on the lower surface of leaves. Sometimes several spots coalesce together to form large lesions. On fruits, symptoms appear as slightly depressed, almost circular, brown to black lesions on the surface. Sometimes concentric rings are formed on some spots. Ultimately, whole infected fruits become rotted (Plate 1 F).

Cercospora ziziphi: Cercospora ziziphi (Plate II A & B) was isolated from leaf samples. Sometimes it was found on leaves as mixed infection with other fungi like Pestalotiopsis. Symptoms appeared on leaves as circular to oval lesions with yellow halo. Initially, spots are yellow and later turn into brown. Finally, spots are surrounded by a dark brown margin. In course of time, spots become larger and visible on both sides of the leaves (Plate II C).

Colletotrichum gloeosporioides: Colletotrichum gloeosporioides was isolated from fruit and leaf samples of jujube. The fungus produces disc-shaped or cushion-shaped and waxy acervuli (Plate III A) containing simple conidiophores bearing conidia. The conidia are hyaline, 1-celled (Plate III B). Under natural conditions, it infects immature fruits causing anthracnose symptoms (Plate III C). Initial symptom of the disease appears as black sunken lesions. On inoculated fruits, the pathogen develops characteristic symptoms of anthracnose (Plate III D).

Curvularia lunata: Curvularia lunata was isolated from fruit, leaf, stem and inflorescence samples (Plate IV A). It was found on fruits as mixed infection with other fungi. Due to its infection, dark brown to black irregular lesions are observed on lower surface of leaves (Plate IV B). The upper surface of infected leaves become yellow. Black depressed spots are found on fruits (Plate IV C).

Isariopsis indica var. ziziphi: The fungus was isolated from only leaf samples. It causes black leaf spot or Isariopsis mold on leaf (Plate VI A). The characteristic symptoms of the disease are sooty tuft-like circular to irregular black spots on ventral surface of leaves. Later, it covers the entire lower surface of leaves giving a sooty appearance (Plate VI B). Septate, dark mycelium and dark synnemata bearing dark conidia form sooty mold (Plate VI C).

Lasiodiplodia theobromae: The pathogen was isolated from fruit samples and leaf samples and identified based on characteristics of mycelia and spore (Plate VII A, B & C). This was found on infected fruits as mixed infection with P. plamarum, C. gloeosporioides, F. semitectum and A. alternata. L. theobromae. The pathogen causes spots on leaves and fruits (Plate VII D & E) under natural condition as well as inoculated condition (Plate VII F).

Mitteriella ziziphina: Mitteriella ziziphina (Plate VIII A & B) was isolated from fruit and leaf samples. The fungus develops almost round and black spots on leaves (Plate VIII C & C(a)) and fruits under natural (Plate VIII D & E) as well as inoculated conditions (Plate VIII F). At advanced stage of infection, severely infected fruits become black and superficial black fungal growth is found on leaves and fruits (Plate VIII C, D & E).

Nigrospora oryzae: The pathogen was isolated from infected fruits samples. It was found on fruits as mixed infection with Alternaria, Lasiodiplodia, Fusarium and Colletotrichum. The pathogen causes black discoloration on both young and mature fruits (Plate IX A & B). Apex of the immature fruits becomes shriveled, rotted and ultimately fruit dropping occurs.

Pestalotiopsis palmarum: Pestalotiopsis palmarum was isolated from infected leaf, fruit and stem samples and it was identified based on conidia with appendages (Plate X B). The fungus causes leaf spot (Plate X C) and gummosis or stem bleeding diseases (Plate X D). Under natural conditions, irregular brown to dark brown lesions with black dot of acervuli were observed on infected leaves (Plate X C). Fruit spot and fruit rot were also observed (Plate XI D). Spots are brown to dark brown in color, raised and corky.  Infected stem becomes rotted and gum like substance comes out from the infected area causing gummosis (Plate X E). Inoculated fruits also formed symptoms similar to natural symptoms (Plate XI C).

Phomopsis sp.: Phomopsis sp. was isolated from diseased fruit samples mixed infection with P. palmarum, C. gloeosporioides and A. alternata. Due to infection of Phomopsis, initially black dot like water soaked small spots appear on fruits. Later, the spot size increases gradually and several spots coalesce together and form large lesion (Plate XI A). At later stage, fruits become soft and rotted and fruit color turns into pale brown. Pycnidia develop on PDA culture (Plate XI B). Sometimes dot like black pycnidia are found on lesions.  Characteristic alpha and beta conidia were observed under microscope (Plate XI C).

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Findings of the present investigation reveal that leaf spots, fruit spots and pre-harvest and post-harvest fruit rot, sooty mould or black mold or Isariopsis mold and stem bleeding or gummosis are common diseases of high yielding jujube varieties in Bangladesh. After harvest jujube fruits are attacked by A. alternata, Aspergillus spp., C. gloeosporioides, C. lunata, F. semitectum, L. theobromae, Nigrospora sp., Penicillium spp., Phomopsis sp., P. palmarum and Rhizopus sp. causing post harvested fruit rot.    The diseases and their causal fungi recorded in Bangladesh also occur in other jujube growing countries of the world. In India, jujube plants are attacked by powdery mildew (O. erysiphoides var. ziziphi), sooty mold (I. inidica var. ziziphi), and leaf spots caused by A. alternata, Cercospora, Septoria, Cladosporium, Pestalotiopsis (Jamadar et al. 2009) and P. palmarum (Madan and Gupta 1976, Rai et al. 1982). From China, Yuan et al. (2009) reported that jujube trees are attacked by powdery mildew, anthracnose (C. gloeosporioides), black spot (A. alternata) and brown spot (P. mauritiana). Jujube fruits are attacked by A. chartarum, A. nanus, A. parasiticus, H. atroolivaceum, P. hessarensis, and S. valparadisiacum. Fruit rots are caused by Fusarium spp., N. oryzae, Epicoccum nigrum, and Glomerella cingulata. Of the diseases only anthracnose (C. gloeosporioides) has been reported earlier from Bangladesh (Rahman et al. (2011).

Based on findings of the present investigation, it may be concluded that 16 fungal plant pathogens are associated with improved and high yielding varieties of jujube diseases in Bangladesh. They cause leaf spots, rust, fruit spots and fruit rot, powdery mildew, sooty mold, stem bleeding and post-harvest deterioration of the fruits. Among the fungal pathogens of jujube A. alternata, C. ziziphi, C. gloeosporioides, C. lunata, F. semitectum, I. indica var. ziziphi, L. theobromae, M. ziziphina, Nigrospora sp. and Phomopsis sp. are recorded as new pathogens of the fruit in Bangladesh

 

LITERATURE CITED

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Khan, A. Z. M., Ali, N. and Shamsi, S. 1983.  Cercosporae from Bangladesh II. Bangladesh J. Bot. 12 (2) : 105-118.

Kuliev, A. A. and Guseinova, N. K. 1974. The content of vitamin C, B1, B2 and E in some fruits. Referativnyi Zhurnal, 2: 69-73.

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Omar, A. Abdul Wahid. 20001. Occurrence of Colletotrichum anthracnose disease of guava fruit in Egypt. Internl. J. Pest Mgt. 47 (2):147-152.

Quin, G. Z. and Tian, S. P. 2004. Biocontrol of post-harvest diseases of jujube fruit by Cryptococcus laurentii combined with a low dosage of fungicides under different storage conditions. Plant Dis. 88(5): 497-501

Rahman, M. M. E., Dey, T. K. and Islam, M. M. 2011. Anthracnose (Colletotrichum gloeosporioides) – a new disease of jujube. Bangladesh J. Plant Pathol. 27(1&2):67-86.

Rai, R. N., Arya, A. and Lal, B. 1982. Pestalotiopis rot of ber (Ziziphus mauritiana). Indian Phytopathology, 35: 709-710.

Sharma, M. V., Majumder, I. and Sharma, M. 1993. Some new post-harvest diseases of ber fruits in India. Indian Phytopathol. 46:415

Singh, U. P. and Singh, H. S. 1979. Occurrence of Fusarium decemcellulare on living galls of Ziziphus mauritiana in India. Mycologia 70: 1126-1129.

Sutton, B. C. 1980. The Coelomycetes. Fungi Imperfecti with Pycnidia, Acervuli and Stromata. Commonwealth Mycological Institute.  Kew, Surrey, England. 696 p.

Yuan, G., Q. Li, Q. Q., Wei, J. G., Lai, C. Y. 2009. Identification of the pathogens of different diseases of Yunnan jujube Zizyphus mauritiana. South China Fruits (3): 57-59.

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1 Senior Scientific Officer, Bangladesh Agricultural Research Institute (BARI), Joydebpur, Gazipur-1701.
2Professors, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur-1706, Bangladesh

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