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Potential of Yeasts As Biocontrol Agents of the Phytopathogen Causing Cacao Witches' Broom Disease

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Potential of Yeasts As Biocontrol Agents of the Phytopathogen Causing Cacao Witches' Broom Disease fmicb-10-01766 July 30, 2019 Time: 15:35 # 1 REVIEW published: 31 July 2019 doi: 10.3389/fmicb.2019.01766 Potential of Yeasts as Biocontrol Agents of the Phytopathogen Causing Cacao Witches’ Broom Disease: Is Microbial Warfare a Solution? Pedro Ferraz1,2, Fernanda Cássio1,2 and Cândida Lucas1,2* 1 Institute of Science and Innovation for Bio-Sustainability, University of Minho, Braga, Portugal, 2 Centre of Molecular and Environmental Biology, University of Minho, Braga, Portugal Edited by: Sibao Wang, Plant diseases caused by fungal pathogens are responsible for major crop losses Shanghai Institutes for Biological worldwide, with a significant socio-economic impact on the life of millions of people Sciences (CAS), China who depend on agriculture-exclusive economy. This is the case of the Witches’ Reviewed by: Mika Tapio Tarkka, Broom Disease (WBD) affecting cacao plant and fruit in South and Central America. Helmholtz Centre for Environmental The severity and extent of this disease is prospected to impact the growing global Research (UFZ), Germany chocolate market in a few decades. WBD is caused by the basidiomycete fungus Ram Prasad, Amity University, India Moniliophthora perniciosa. The methods used to contain the fungus mainly rely on *Correspondence: chemical fungicides, such as copper-based compounds or azoles. Not only are these Cândida Lucas highly ineffective, but also their utilization is increasingly restricted by the cacao industry, [email protected] in part because it promotes fungal resistance, in part related to consumers’ health Specialty section: concerns and environmental awareness. Therefore, the disease is being currently This article was submitted to tentatively controlled through phytosanitary pruning, although the full removal of infected Fungi and Their Interactions, a section of the journal plant material is impossible and the fungus maintains persistent inoculum in the soil, Frontiers in Microbiology or using an endophytic fungal parasite of Moniliophthora perniciosa which production Received: 07 March 2019 is not sustainable. The growth of Moniliophthora perniciosa was reported as being Accepted: 17 July 2019 antagonized in vitro by some yeasts, which suggests that they could be used as Published: 31 July 2019 biological control agents, suppressing the fungus multiplication and containing its Citation: Ferraz P, Cássio F and Lucas C spread. Concurrently, some yeast-based products are used in the protection of fruits (2019) Potential of Yeasts as from postharvest fungal spoilage, and the extension of diverse food products shelf-life. Biocontrol Agents of the Phytopathogen Causing Cacao These successful applications suggest that yeasts can be regarded a serious alternative Witches’ Broom Disease: Is Microbial also in the pre-harvest management of WBD and other fungal plant diseases. Yeasts’ Warfare a Solution? GRAS (Generally Recognized as Safe) nature adds to their appropriateness for field Front. Microbiol. 10:1766. doi: 10.3389/fmicb.2019.01766 application, not raising major ecological concerns as do the present more aggressive Frontiers in Microbiology| www.frontiersin.org 1 July 2019| Volume 10| Article 1766 fmicb-10-01766 July 30, 2019 Time: 15:35 # 2 Ferraz et al. Yeast-Based Biocontrol of Cacao Phytopathogen approaches. Importantly, mitigating WBD, in a sustainable manner, would predictably have a high socioeconomic impact, contributing to diminish poverty in the cacao- producing rural communities severely affected by the disease. This review discusses the importance/advantages and the challenges that such a strategy would have for WBD containment, and presents the available information on the molecular and cellular mechanisms underlying fungi antagonism by yeasts. Keywords: Witches’ Broom Disease, Moniliophthora perniciosa, yeasts, biocide, antagonism, sustainability, cacao, phytopathogen INTRODUCTION Phillips-Mora, 2005) (formerly designated Crinipellis perniciosa). The severity and extent of its manifestation is endangering the A great number of plant diseases are responsible for major crop rapidly expanding and very quality-demanding chocolate market. losses with huge socio-economic impact, causing each year a This review focuses on this disease, the methodologies presently worldwide estimated losses of 40 billion dollars (Syed Ab Rahman used for containment, and the innovative approaches that could et al., 2018). Particularly, the diseases caused by fungal pathogens be explored (Figure 1). are increasingly recognized as a global threat to food production and security. In fact, since 2000 the number of new fungal plant pathogen alerts has increased by more than sevenfold (Fisher WITCHES’ BROOM DISEASE OF CACAO et al., 2012). Presently, fungal-generated diseases constitute 64– 67% of the total crop diseases reported globally (Fisher et al., According to data from the International Cacao Organization1, 2012; Fisher et al., 2018), and account for 20% of the losses at the more than 4 million tons of cacao beans are produced annually level of production and a further 10% at postharvest level (Fisher (Wickramasuriya and Dunwell, 2018). Cacao beans are the core et al., 2018). These authors estimate that fungal diseases are raw material for the chocolate industry, although other cacao- spreading northbound at a rate of almost 8 km/year. This could derived products also have important world markets, such as derive from increasingly common agricultural practices, such as cacao butter or liquor (Pohlan and Pérez, 2010; Wickramasuriya the extensive monocultures and the use of a restricted number and Dunwell, 2018). The economic global market for chocolate of plant cultivars, as well as the increased global international reached US$ 110 billion in 2015, and the world demand is trade proportionating disease spreading over great distances expected to grow exponentially in the next decade due to the (Fisher et al., 2012). Climate change adds a burden to that globalization of consumption styles in expanding economies such equation, potentiating the development of microbes and vectors as China and India (Squicciarini and Swinnen, 2016). Cacao is in unprecedented regions (Robert et al., 2015; Fisher et al., 2018). produced in countries located approximately in the same latitude To prevent plant diseases and protect crops from pests and interval of equatorial climate, forming the so-called Cacao Belt pathogens, widely spread methodologies mainly correspond to (Pohlan and Pérez, 2010). The biggest producers are therefore applying chemical fungicides. The continued use of chemical countries from Central and South America and Africa. The cacao fungicides leads to the development of fungicide resistance in plant is affected by several diseases, the more threatening of the fungal pathogen (Syed Ab Rahman et al., 2018) and, in which is WBD (Purdy and Schmidt, 1996; Pereira, 1999; Griffith the absence of other control measures, to the re-emergence of et al., 2003; Aime and Phillips-Mora, 2005; Teixeira et al., 2015). virulence (Fisher et al., 2018). Therefore, in spite that the use This has severely affected South and Central America countries, of pesticides brought clear improvements in crop quality and where it has been responsible for major irreversible crop losses. quantity during more than half a century, their progressive The highest economic and social consequences of WBD are inefficacy to treat some of the most harmful plant diseases described to have occurred in Brazil. In the 10 years after the requires the utilization of higher dosages each year (Medeiros onset of the disease in 1989, WBD reduced the cacao production et al., 2010; Syed Ab Rahman et al., 2018). The use of fungicides in more than 70% (Pereira et al., 1989; Santos Filho et al., 1998; heavily impacts on the microflora of agrarian ecosystems, Trevizan and Marques, 2002; Meinhardt et al., 2008; Pires et al., destroying beneficial microbes, such as endophytic bacteria and 2009; Teixeira et al., 2015), causing Brazil to shift from being fungi, as well as animals important for the quality of the soils the 2nd world producer to becoming a net importer of cacao (Syed Ab Rahman et al., 2018). Ultimately, the systemic use beans (Bowers et al., 2001; Marelli et al., 2009; Teixeira et al., of these drugs leads to the persistence of chemical residues 2015). During that period, the most affected region of Bahia in the environment, proportionating low dosage toxicity and suffered losses around 90%, configuring a severe social crisis from contaminating species across trophic levels (Carvalho, 2006; losing more than 200,000 farm jobs (Trevizan and Marques, 2002; Dukare et al., 2018). Teixeira et al., 2015). One of the fungal diseases with recognized high negative The severity of WBD derives from several factors. socio-economic impact is the pathology of cacao plant and fruit Moniliophthora perniciosa does not form specialized infection known as Witches’ Broom Disease (WBD). This is caused by the basidiomycete fungus Moniliophthora perniciosa (Aime and 1www.ICCO.org Frontiers in Microbiology| www.frontiersin.org 2 July 2019| Volume 10| Article 1766 fmicb-10-01766 July 30, 2019 Time: 15:35 # 3 Ferraz et al. Yeast-Based Biocontrol of Cacao Phytopathogen FIGURE 1 | Diagram presenting the challenges posed by WBD and the opportunities that natural antagonistic yeasts present for the containment of the disease. Cacao plant figure adapted from Panhuys, L. von, Watercolours of Surinam (1811–1824) (source: (CC) BY-NC-ND http://plantillustrations. org/illustration.php?id_illustration=190533).
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