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Two New Species of Fusarium Section Liseola Associated with Mango Malformation

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Two New Species of Fusarium Section Liseola Associated with Mango Malformation Mycologia, 94(4), 2002, pp. 722±730. q 2002 by The Mycological Society of America, Lawrence, KS 66044-8897 Two new species of Fusarium section Liseola associated with mango malformation Henriette Britz1 two new taxa in the section Liseola that we have Emma T. Steenkamp named F. mangiferae and F. sterilihyphosum. Fusarium Teresa A. Coutinho2 mangiferae is conspeci®c with strains that were pre- Department of Microbiology and Plant Pathology, viously identi®ed as F. subglutinans and reported to Forestry and Agricultural Biotechnology Institute be the causal agent of malformation in mango grow- (FABI), University of Pretoria, Pretoria 0002, ing areas throughout the world. Fusarium sterilihy- South Africa phosum, on the other hand, has been isolated only Brenda D. Wing®eld from malformed mango tissue in South Africa. Department of Genetics, Forestry and Agricultural Key Words: Gibberella fujikuroi complex, mango, Biotechnology Institute (FABI), University of Pretoria, taxonomy Pretoria 0002, South Africa Walter F. O. Marasas Programme on Mycotoxins and Experimental INTRODUCTION Carcinogenesis (PROMEC), Medical Research Council (MRC), P.O. Box 19070, Tygerberg, South Africa Mango (Mangifera indica L.) malformation is an eco- nomically important disease in mango-growing areas Michael J. Wing®eld of the world including India, Pakistan, Egypt, South Forestry and Agricultural Biotechnology Institute Africa, Brazil, Israel, Florida, and Mexico (Kumar et (FABI), University of Pretoria, Pretoria 0002, South Africa al 1993, Freeman et al 1999). This disease causes ab- normal development of vegetative shoots and in¯o- rescences (Kumar et al 1993). Floral malformation is Abstract: Mango malformation is an economically the most prominent symptom and is characterized by important disease of Mangifera indica globally. A re- abnormal, thick and ¯eshy panicles (Varma 1983, Ku- cent DNA-based study indicated that two distinct, mar et al 1993). Affected panicles bear no fruit, re- phylogenetic lineages previously identi®ed as Fusari- sulting in signi®cant economic losses (Varma et al um subglutinans are associated with this disease in 1974, Varma 1983, Kumar et al 1993). South Africa. The objective of this study was to char- The etiology of mango malformation disease is acterize Fusarium isolates associated with mango mal- controversial. Physiological abnormality, virus infec- formation, including the two different F. subglutinans tions, mite infestations and fungal pathogens have groups, based on morphological characteristics. For been reported as the causal agents of this disease this purpose we examined Fusarium strains isolated (Kumar et al 1993). Summanwar et al (1966) iden- from diseased mango in¯orescences from diverse ti®ed the fungal pathogen commonly associated with geographical origins. We also used sexual compati- the disease as Fusarium subglutinans (Wollenweber & bility tests to determine whether sexual reproduction Reinking) Nelson, Toussoun & Marasas (5 F. moni- among the strains was possible. The morphological liforme Sheldon var. subglutinans Wollenweber & Re- characters considered were shape of the conidia, inking), residing in section Liseola. Freeman et al presence of mono- and/or polyphialides, origin of (1999) recently demonstrated that isolates identi®ed the conidiophores from the substrate, presence of as F. subglutinans induced typical mango malforma- chlamydospores and the presence of sterile coiled hy- tion symptoms on mango trees using the isolate MRC phae. Three unique Fusarium spp. were identi®ed. 7559 (506/2) originally collected from mango in¯o- In this paper, we provide formal descriptions for the rescences in Israel. Fusarium subglutinans forms part of the Gibberella Accepted for publication December 15, 2001. fujikuroi (Sawada) Ito in Ito & K. Kimura species 1 Present address: Onderstepoort Veterinary Institute, Private Bag complex (Leslie 1995, Britz et al 1999). Fusarium X5, Onderstepoort, 0110, South Africa. subglutinans sensu lato is, however, a polyphyletic tax- 2 Corresponding author, mailing address: Forestry and Agricultural on that has been associated with various plant hosts, Biotechnology Institute (FABI), University of Pretoria, Pretoria 0002, South Africa. Phone (27 12) 420 3938, Fax (27 12) 420 3960. each of which represents a distinct lineage in the G. Email: [email protected] fujikuroi complex (Leslie 1995, O'Donnell et al 1998, 722 BRITZ ET AL: FUSARIUM SPP. ASSOCIATED WITH MANGO MALFORMATION 723 Britz et al 1999, Steenkamp et al 1999, 2000a, Agricultural Biotechnology Institute (FABI), University of O'Donnell et al 2000). These lineages are dif®cult to Pretoria, Pretoria, South Africa and the culture collection distinguish using conventional morphological char- of the Medical Research Council (MRC), P.O. Box 19070, acters such as those proposed by Nelson et al (1983). Tygerberg, South Africa. Until relatively recently, these fungi were distin- Mango in¯orescence clusters collected in South Africa guished from each other using pathogenicity and were surface sterilized with 70% ethanol for 2 min and mating studies (Leslie 1995). The different lineages washed with sterile deionized water for 1 min. Single mal- representing F. subglutinans sensu lato are, however, formed ¯owers were removed from the sterilized cluster and plated onto a Fusarium selective medium (Nash and readily distinguishable using DNA sequences of Snyder 1962). After incubation for 5 d at 25 C, small agar genes for b-tubulin, translation elongation factor EF- pieces overgrown with mycelium were taken from the edges 1a, histone H3, and calmodulin (O'Donnell et al of the colonies and transferred to 90 mm diameter Petri 1998, Steenkamp et al 1999, 2000a, O'Donnell et al dishes containing carnation leaf agar (CLA) (Fisher et al 2000). 1982). After incubation on CLA at 25 C for 7 d, single co- Mango malformation in South Africa is associated nidial isolates were prepared and stored in 15% glycerol at with two phylogenetically distinct groups of isolates 270 C. until recently referred to as F. subglutinans (Steen- To stimulate culture and conidial development, Fusarium kamp et al 1999, 2000a). Based on the histone H3 isolates (TABLE I) were transferred to CLA (Fisher et al and b-tubulin gene sequences, one group of isolates 1982) and KCl agar (Nelson et al 1983). Cultures were in- represents a previously undescribed lineage in the G. cubated at 23 C under ¯uorescent and cool-white light with fujikuroi complex. The second group of isolates is a 12 h photoperiod. After 10 to 14 d of incubation, the conspeci®c with isolates that were previously report- following morphological characters were examined: shape ed to be the causal agent of mango malformation of the conidia, presence of mono- and/or polyphialides, (Steenkamp et al 2000a). The results presented by origin of the conidiophores from the substrate, presence of these authors also con®rmed those of Viljoen et al chlamydospores and sterile coiled hyphae (Nirenberg and (1997), O'Donnell et al (2000) and Leslie (pers O'Donnell 1998). Secondary characteristics such as growth comm), who have shown using random ampli®ed rate and colony color (Rayner 1970) were determined on polymorphic DNA (RAPDs), DNA sequence of sev- potato dextrose agar (PDA) after incubation at 25 C in the dark (Nelson et al 1983) for the two newly described spe- eral genes, and isozymes, respectively, that mango cies. Each isolate was plated onto three different PDA plates malformation is associated with two distinct species, and the growth rate was determined over a period of 10 d. both with morphological characters typical of F. sub- This entire procedure was repeated once more. A one way glutinans. ANOVA was done to determine whether growth rate dif- The aim of this study was to characterize, using fered signi®cantly for the different isolates. Colony color morphology, Fusarium spp. isolated from malforma- was determined after 14 d using the color coding system of tion mango tissue from diverse geographical origins. Rayner (1970). Fifty measurements were made of all diag- For this purpose the morphological characteristics nostic morphological characters. The measurements are in- proposed by Nirenberg and O'Donnell (1998) were dicated as minimum, mean, and maximum. used. Sexual compatibility tests were also used to ver- ify the identity of some of these Fusarium spp. Mating type and sexual compatibility tests. The mating type (MAT-1 or MAT-2) of all the isolates included in this study were determined using the PCR-based method described by MATERIALS AND METHODS Steenkamp et al (2000b). Only isolates with opposite mat- ing types were crossed within each species and between spe- Morphological and cultural studies. Fusarium spp. associ- cies using the method described by Klittich and Leslie ated with mango malformation in South Africa were isolat- (1988) with some modi®cations (Britz et al 1999). Covert ed from mango trees in Tzaneen (Northern Province), et al (1999) found that a lower incubation temperature in- which included the areas Letsitele (LS) and Deer Park (DP). Isolates were also collected from Nelspruit (NS), Fre- creased sexual fertility among isolates of G. circinata Niren- denheim (FH), Malelane (ML) and Hazyview (HZ) (Mpu- berg & O'Donnell. We, therefore, used an incubation tem- malanga). Other isolates used in this study were isolated perature of 17 C for our crosses. Sexual crosses have already from malformed mango tissue by other collectors in Flori- been performed within and between
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