Fungi on Commelina Benghalensis from Brazil, with Notes on Potential for Weed Biological Control
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Trop. plant pathol. (2018) 43:21–35 DOI 10.1007/s40858-017-0189-6 ORIGINAL ARTICLE Fungi on Commelina benghalensis from Brazil, with notes on potential for weed biological control Bruno W. Ferreira1 & Janaina L. Alves1 & Bruno E. C. Miranda1 & Robert W. Barreto1 Received: 6 February 2017 /Accepted: 11 September 2017 /Published online: 4 October 2017 # Sociedade Brasileira de Fitopatologia 2017 Abstract Commelina benghalensis (tropical spiderwort - TS) that such exotic fungi, may offer a valuable resource for man- is an invasive herbaceous plant, native to South and Southeast agement of one of the worst agricultural weeds in Brazil and in Asia and one of the worst agricultural weeds in the tropics. Its the tropical world, and require investigation as biological con- management is notoriously difficult because of its ability to trol agents for introduction in Brazil. regenerate from small fragments and its tolerance to glypho- sate applications. There are no published records of biocontrol Keywords Biological control . Commelinaceae . fungal attempts against TS involving either microbial or arthropod pathogens . taxonomy natural enemies. Prior to investigating classical biocontrol agents, surveys have been conducted in Brazil and, more re- cently, concentrated in Viçosa (state of Minas Gerais) to de- Introduction termine whether fungal pathogens of TS are already present. Five different fungal pathogens were collected. These fungi Commelina benghalensis (Commelinaceae) is an herbaceous were identified as causing the following diseases: Athelia perennial plant native to South and Southeast Asia. It is rolfsii – crown rot, Cercospora cf. sigesbeckiae – leaf spots, known by several common names, among them tropical spi- Corynespora cassiicola – leaf spots, Neopyricularia obtusa derwort (TS), wandering Jew, and trapoeraba in Brazil. It is sp. nov. – leaf spots and Rhizoctonia solani – blight. One of widely distributed in tropical and subtropical regions of the the fungi found on TS represents a new taxon, and the others world (Kissmann 1991). TS reproduces both by true seeds and represent either a new host association, a new geographic by vegetative propagation. When its stems are cut into pieces, record or both, except for Corynespora cassiicola,which they rapidly regenerate giving rise to new plants, facilitating has already been recorded as able to attack TS (ex-tomato the dissemination and perpetuation of the weed in infested isolates, under controlled conditions) in Brazil. The areas (Holm et al. 1977). TS is regarded as one of the world’s mycobiota identified in Brazil is limited and lacks many of worst weeds, affecting 25 crops in 29 countries (Holm et al. the TS-specific fungal pathogens recorded in Africa and Asia, 1977; Webster et al. 2005). In Brazil, it has been reported namely: Kordyana celebensis, Kordyana indica, Phakopsora causing serious problems in soybean and coffee plants. tecta, Puccinia commelinae, Uredo ochracea, Bauerago Infestations of soybean fields lead to reduced production of combensis and Bauerago commelinae. It is conjectured here, grain, difficulties in harvest operations, and depreciation of the grain rating, due to increased moisture content (Kissmann 1991). A single TS plant can produce up to 1600 seeds, which along with its rapid reproductive rate, may cause the formation Section Editor: Alan R. Wood of dense and uniform stands that completely smother other * Robert W. Barreto plants, especially young or small sized species (Holm et al. [email protected] 1977). TS has a membranous sheath enveloping its axillary buds, which prevents the direct contact of these regenerative 1 Departamento de Fitopatologia, Universidade Federal de Viçosa, tissues with herbicides, hindering their absorption and making Viçosa, Minas Gerais 36570-900, Brazil chemical control less efficient. TS also produces seeds from 22 Trop. plant pathol. (2018) 43:21–35 cleistogamous hypogeous flowers formed from the rhizomes in Brazil. Specimens of Phoma sp. and Curvularia sp. were which are slightly larger than the seeds produced by aerial never collected again after the survey in the state of Rio de flowers and which are able to germinate and emerge from Janeiro, suggesting that they may represent just occasional up to 12 cm underground, diminishing the efficiency of pre- occurrence of opportunists or saprophytes. Unfortunately, emergence herbicide applications (Kissmann 1991). the work was discontinued without achieving a complete iden- Strangely, although Ellison and Barreto (2004)considered tification of fungi collected in the surveys and the specimens TS as a potential candidate to become a biocontrol target in were lost. More recently, during a local survey in the munic- Latin America, and Evans (1987) considered some pathogenic ipality of Viçosa, in the state of Minas Gerais, Brazil, it was fungi known to attack TS as having good potential for use as found that most of the fungi collected in previous years were classical biocontrol agents, there are still no published records present and available for a more detailed examination. Here, of attempts to target TS for biological control with either ar- the identity of the collected fungi is reported and a comparison thropod or microbial natural enemies. Nevertheless, a classical of the mycobiota associated with C. benghalensis in Brazil biological control program is being conducted against another and the Old World is provided, with comments on their po- member of the family Commelinaceae during recent years, tential use in weed biocontrol in the future. namely Tradescantia fluminensis, a neotropical species that became a noxious environmental weed in New Zealand and Australia after being introduced as an ornamental plant. Materials and methods Several arthropods species have already been introduced against T. fluminensis in New Zealand (Fowler et al. 2013). A provisional list of fungi collected from TS in the state of Rio Also, the fungus Kordyana brasiliensis, recently described by de Janeiro, along with many other weedy hosts has been pub- Macedo et al. (2016), is being evaluated for its release in lished (Barreto and Evans 1995a), but numerous ad hoc col- Australia and New Zealand (Morin 2015). The use of natural lections were also performed since those early days. The sam- enemies collected in the native range of TS in the Old World ples included in this study were collected in the campus of the (classical biological control) is an attractive alternative for bio- Universidade Federal de Viçosa (Viçosa, state of Minas logical control, providing they are damaging to, co-evolved with, Gerais, Brazil) and its vicinities, in crop and pasture areas as and host-specific to TS, and have remained restricted to those well as in ruderal situations such as roadsides, abandoned areas. Natural enemies with such characteristics could be intro- areas, and gardens where TS occurred. They were dried in a duced into regions where TS became a noxious weed. This ap- plant press and later transferred to paper envelopes and depos- proach has a long history, with many examples of success and an ited in the herbarium of the Universidade Federal de Viçosa excellent safety record (Barton 2004). (Herbarium VIC). The samples were carefully examined un- Concepts and examples of the application of pathogens as der a stereoscopic microscope and fungal structures that ap- weed biocontrol agents have been recently reviewed by peared associated with disease symptoms were isolated with a Barreto et al. (2012). Among the first steps of classical bio- sterile fine pointed needle and, whenever possible, directly control programs against weeds, is surveying the area where transferred onto plates containing vegetable broth-agar the weed problem occurs in order to “avoid a later, superfluous (VBA), as described by Pereira et al. (2003). Pure cultures (and also wasteful and potentially embarrassing) introduction were preserved in potato carrot-agar (PCA) tubes, in silica- of natural enemies that may be already present, but were inef- gel, as described in Dhingra and Sinclair (1996)orin fective and, hence, remained unnoticed in the target area” cryotubes containing 10% glycerol stored at -80 °C. Pure cul- (Barreto et al. 2012). TS was included as a target weed in a tures were deposited in the culture collection of the survey performed in the late 1980s, concentrated in the state of Departamento de Fitopatologia of the Universidade Federal Rio de Janeiro (Barreto 1991). Numerous samples of diseased de Viçosa (COAD). TS plants were collected at many sites, but only a preliminary Observations of the morphology of the fungi were examination of the material was possible at the time, and only made on slides containing free hand sections or fungal four fungi were recorded as associated with diseased tissue material scraped from the diseased tissues mounted in (Barreto and Evans 1995a). At the time, those fungi were lactoglycerol or lactofuchsin. Measurements and illustra- identified at the genus level only, and belonged to Bipolaris tions (photomicrographs) were prepared with an sp. (later identified as Corynespora), Cercospora sp., Olympus BX 51 light microscope fitted with a drawing tube Curvularia sp., and Phoma sp. Since then, numerous later and an Olympus E330 camera. Culture descriptions were based ad hoc collections in other Brazilian states were conducted, on the observation of 11-day-old colonies formed in plates con- but the list of fungi associated with diseased TS tissue did not taining either potato dextrose-agar (PDA) or PCA maintained at increase. In fact, the results of these surveys showed that 25 °C under a 12-h daily/light regime (light provided by two Corynespora was the most common fungal pathogen of TS white and one near-UV lamps placed 35 cm above the plates) or Trop. plant pathol. (2018) 43:21–35 23 in the dark (plates wrapped in aluminum foil). The color termi- In culture: Fast growing colonies (90 mm diam after 4 days) nology follows Rayner (1970). composed of white aerial mycelium, sparse and felty, sclerotia Genomic DNAwas extracted from each culture by growing formed on the surface of the colonies after 15 days; not the fungus on PDA plates for 10 days at 24 °C and removing sporulating.