Introduction

The twentieth century agricultural research focused on the problem of increasing crop productivity vis-à-vis the upsurge in world population and demand for food (Evans 1998; Nellemann et al. 2009). However, the twenty-first century is faced with an unprecedented problem of global food security and food safety. Most insidiously, more than 800 million people lack adequate food and 1.3 billion live on less than $1 USD a day (James 1998; FAO 2000; Christou and Twyman 2004). Although Cochliobolus (anamorph Bipolaris/Curvularia) species are important in crop pathogenesis (Acharya et al. 2011; Ohm et al. 2012; Louis et al. 2015), they are seed-borne (Ji et al. 2011) and produce toxins (Desjardins and Hohn 1997; Rhoads et al. 1995; Wu et al. 2012; Condon et al. 2013, 2014b; Nawas et al. 2017). Hence, Cochliobolus species affect nutrition security. According to FAO 2012 draft formulation, nutrition security only exists when all people at all times consume food of sufficient quantity and quality in terms of variety, diversity, nutrient content and safety to meet their dietary needs and food preferences for an active and healthy life, coupled with a sanitary environment, adequate health, education and care (CFS 2012). Arguably, food security has never been achieved worldwide even when political will is fully established; food insecurity still emerges in different regions as a result of compounding variabilities in abiotic and biotic factors. While humans cannot fully manage abiotic uncertainties such as climate change and extreme weather events, biotic factors are often manipulated to overcome food insecurity at the production level.

According to Harlan (1995), maize (Zea mays), pearl millet (Pennisetum glaucum) sorghum (Sorghum bicolor), wheat (Triticum aestivum), rice (Oryza sativa) and potato (Solanum tuberosum) are important for global human consumption. Therefore, crop destroyers such as viruses, bacteria, nematodes and fungi (herein referred as phytopathogens) that significantly hamper the production of wheat, rice, maize, millet, sorghum and potato create disequilibrium in the strategic balance in nutrition security. It is estimated that phytopathogens account for persistent yield losses of about 20% of world’s harvest, with an additional 10% post-harvest loss (Oerke 2006). Ideally, complete control of plant fungal diseases occurring in major world crops could allow feeding of over 600 million people annually (Fisher et al. 2012).

Although losses caused by the genus Cochliobolus have been ignored in the last 50 years, the economic implications on human and animal health (Madrid et al. 2014; Yew et al. 2014; Bengyella et al. 2017) and crop losses on global nutrition security are substantial (Liu and Wang 1999; Li et al. 2004, 2006). The genus Cochliobolus since their detailed taxonomy in the 1930s (Drechsler 1934) has undergone multiple taxonomic re-evaluations (Manamgoda et al. 2011, 2012; Rossman et al. 2015). The fungal genus Cochliobolus include 55 species containing well-known plant pathogenic species such as Cochliobolus carbonum, C. heterostrophus, C. miyabeanus, C. sativus and C. lunatus (Condon et al. 2014a, b; Singh et al. 2014; Iftikhar et al. 2017). Initially thought to be exclusively plant pathogens with complex mode of reproduction, multisporic and overlapping morphological features, focused in the nineteenth and twentieth century, were based on taxonomic delineations (Manamgoda et al. 2011, 2012; Iftikhar et al. 2017). Cochliobolus species gained prominence following the economic and ecologic disaster of the staple crop rice in 1940s in Bengal.

Given the immense social and economic consequences from the past Cochliobolus epidemics (Ullstrup 1972; Scheffer 1997; Walton et al. 1997), genomes of elite species such as C. lunatus, C. heterostrophus, C. sativus, C. victoriae and C. carbonum have been sequenced (Condon et al. 2014a, b; Gao et al. 2014; Bengyella et al. 2017). The impact of these invasive species on the bioeconomy worldwide could be estimated over $US10 billion dollars per annum, considering the implications in the medical (Madrid et al. 2014; Yew et al. 2014) and agricultural (Liu and Wang 1999; Li et al. 2006) industries. Furthermore, the effect of Cochliobolus species on the agricultural sector has caused discrepancies between supply and demand of staple foodstuff such as maize, pearl millet and sorghum in Sub-Saharan Africa and Indian sub-continent (Raemakers 1988; Jones and Jeutong 1993; Sreenivas et al. 2010; Acharya et al. 2011). Dismal imbalances in food supply are not new (Dyson 1999); nonetheless, inadequate consideration of the impact of the genus Cochliobolus on food crops could cause severe health and economic hardship especially to farmers’ subsistence, create food insecurity and loss of market value for most crops.

Because of the socioeconomic impact of Cochliobolus diseases, understanding the current dynamics of Cochliobolus species vis-à-vis staple food crops and the rapid changing natural ecosystems including climate change could provide more quality evidence to raise the awareness of invasive species threats and impacts over time. Equally, outlining the distribution of Cochliobolus species in the twenty-first century and the current trends that allow them to thrive successfully and compromise food security in the production perspective would help elaborate appropriate disease management strategies to curb any major disease outbreak. In this paper, we looked into the above issues and stress on the impact of Cochliobolus diseases, consequences of persistent species diversity, lifestyle, evolving pathogenicity, epidemics, distribution and food security issues.

Impact of Cochliobolus diseases on major crops losses

It was estimated that diseases and pest could deprive humanity of up to 50% of major crops (Oerke 2006). Cochliobolus species not only cause damages to field crops, but since they are mainly seed-borne pathogens (Ji et al. 2011) mediate post-harvest damage and reduce market value (Singh et al. 2014). The damage products are often discarded (Ahmed and Ravinder 1993) because of the lack of technology to transform spoiled food into animal feed. Interestingly, Cochliobolus species produce mycotoxins in infected rice (Gangopadhyay and Chakrabarti 1982), making it unfit for consumption and thus jeopardizing food security. Furthermore, because Cochliobolus species produces cytochalasins (Visconti and Sibilia 1994), a molecule that inhibits cytokinesis, protein synthesis and causes pulmonary hemorrhage and brain edema, it calls for unrestricted share of post-harvest preservation technologies between developed and underdeveloped countries. This could particularly be useful to enhance nutrition security in African countries such as Nigeria where the incidence of mycotoxins in rice is reportedly high (Makun et al. 2007).

It was demonstrated that the global food consumption is dominated by four staple crops viz., wheat, rice, maize and potato (Harlan 1995), suggesting they are great stabilizers of the global food security. A greater picture defining the impact of Cochliobolus diseases in the context of growing food insecurity is achievable if one perused how Cochliobolus species affect staple crops and others. Such examination could be of importance in drafting blueprint policy and strategic programs for Cochliobolus diseases. In this regard, we provide the disease profiles of key Cochliobolus species on the production of rice, sorghum, wheat, maize, cassava (Manihot esculenta) and potato:

(i) Common Cochliobolus disease of rice:

  • Rice is the third-highest cash crop in farm production after sugarcane and maize (FAOSTAT 2017). The fungus C. lunatus causes black kernel disease under warm weather and high humidity conditions. Rice is often characterized by dark discoloration of the kernels.

  • Although brown spot disease caused by C. miyabeanus is common in Asia (Nasu et al. 1967), it has been identified in the Western Highlands of Cameroon and drastically reduces rice yield (Jones and Jeutong 1993).

  • Cochliobolus lunatus have been identified as the causative agent of leaf blight disease of rice characterized by leaf-streak symptoms in the Zhejiang Province of China (Liu et al. 2014).

  • Black smudge disease of rice is caused by Bipolaris sorokiniana (Sacc) Shoemaker (sexual stage Cochliobolus sativus) and occurs under high temperature conditions (Nasu 1963).

(ii) Black point and spot blotch disease of wheat: wheat is an important economic crop and wheat global trade is greater than for all other crops combined (Curtis et al. 2002). The fungus C. sativus infects seeds, reduces germination and increases seedling blight. Black point disease could be severe when C. sativus co-infects wheat with other pathogens such as Alternaria species and Fusarium species (Hudec 2007), often resulting in germination retardation and coleoptile growth rate retardation. Furthermore, wheat infection by C. sativus is highly variable, very sensitive to environmental conditions and hallmarked by isolates differing in aggressiveness (Duveiller and Altamirano 2000). Thus, this compromises early detection of black point and spot blotch disease of wheat as well as jeopardizes timely interventions in the implementation of appropriate disease management strategies. Also, significant yield loss from spot blotch disease reported in Zambia stood at 85% (Raemakers 1988), 40% in the Philippines based on field trials (Lapis 1985) and up to 57% in Boliva (CPC 2007).

(iii) Brown spot disease of asparagus: asparagus (Asparagus officinalis) is a vegetable and widely consumed as a delicacy across the world with the top importers in 2003 being the USA (182,805 tons), EU (94,475 tons) and Canada (20,219 tons) (FAOSTAT 2016). Nonetheless, asparagus farming is severely hampered by C. lunatus, C. brachyspora, C. eragrostidis and C. pallescens (Salleh et al. 1996).

(iv) Curvularia cotyledon spot of soybean: the global production of soybean increased reaching approximately 324 million tons in 2016 (FAO 2014; USDA 2016). Nevertheless, the fungus C. lunatus var. aeria causes necrotic lesions on soybean cotyledons and it has been a serious disease of soybean in Minas Gerais, Brazil (Muchovej 1988).

(v) Curvularia leaf spot of maize: corn is the main cereal crop in Sub-Saharan Africa and staple food for about 1.2 billion people (IITA 2009). Curvularia leaf spot disease is common in Nigeria and significantly affects local maize production (Fajemisin and Okuyemi 2009). In Nigeria, it was found that C. pallescens causes Curvularia leaf spot of maize and could be controlled with copper oxychloride + zineb and copper oxychloride (Fajemisin and Okuyemi 2009). In India and China, the same disease is caused by C. clavata and C. australiensis and seriously damages maize leaves (Mandokhot and Chaaudhary 1972; Chang et al. 2016). This means that the different species of fungi of the genus Cochliobolus (teleomorphic state of the anamorphic genera Bipolaris and Curvularia) can produce the same symptoms of the disease.

(vi) Grain mold of sorghum: this is a worldwide disease of sorghum caused by over 40 fungi genera (Navi et al. 1999). Nonetheless, C. lunatus and C. australiensis are predominant pathogens in the genus Cochliobolus with worldwide representation (Navi et al. 1999; Thakur et al. 2003). Production losses due to grain mold of sorghum range between 30 and 100% depending on the cultivar, time of flowering and weather conditions during harvest (Singh and Bandyopadhyay 2000).

(vii) Leaf blight of Job’s tears: Job’s tears are tall grain-bearing tropical plant of the family Poaceae whose seeds are used for ornamental purpose and as medicine and food in many countries (Chang and Hwang 2002). Leaf blight disease of Adlay, a limiting factor in Adlay farming, is caused by Bipolaris coicis (teleomorph: Cochliobolus nisikadoi) (Ahmadpour et al. 2013). Nonetheless, C. nisikodi causes diseases in other crops such as corn, wheat, barley and tiger grass (Sivanesan 1987; Cho and Shin 2004; Manamgoda et al. 2012).

(viii) Seedling blight of sugarcane: sugarcane is an important economic crop and C. lunatus, Drechslera rostrate, D. hawaiiensis and C. senegalensis significantly hinder the propagation of seedlings from true seed (Fuzz) (Byther and Steiner 1971).

(ix) Stem disease of cassava: while DNA and RNA viruses often cause diseases in cassava, severe Curvularia stem blight disease caused by C. lunatus has been observed in Benin, Ghana and Nigeria (Msikita et al. 2007). In susceptible cassava cultivars like TMS30572 and Odongbo under field conditions, shoot sprouting was reduced by 4–18% and 26–58%, respectively, due to infection (Msikita et al. 2007). This fungal disease is of significant economic importance because cassava is a major source of income, employment and foreign exchange in Sub-Saharan Africa (Anderson et al. 2004).

(x) Black-to-brown spot disease of potato: apart from Phytophthora infestans that causes potato late blight and massive yield losses worldwide (Tsedaley 2014; Roy and Grűnward 2014), C. lunatus was shown to cause brown-to-black spot disease of potato in West Bengal, India (Louis et al. 2013; Bengyella et al. 2014).

(xi) Spot blotch disease of barley: spot blotch of barley caused by C. sativus negatively affects yield and quality of barley worldwide. Average yield losses of 16–33% (Clark 1979), 40% (Van Leur 1991) and 20–70% (Karov et al. 2009) have been reported in barley depending on the cultivar. The severity of the spot blotch disease of barley has decreased in the USA following the introduction of highly resistant six-rowed malting barley cultivars (Valjavec-Gratian and Steffenson 1997). Nonetheless, it was suggested that virulent pathotypes of C. sativus could still infect and grow on foliage of resistant barley cultivars in the field (Valjavec-Gratian and Steffenson 1997).

Consequences of persistent diversity of Cochliobolus species on crop production

The genus Cochliobolus falls among the pleomorphic genera in Dothideomycetes (Ohm et al. 2012; Rossman et al. 2015). Substantial efforts have been made to refine the taxonomic placement of Cochliobolus species and equally differentiate them from Bipolaris species (Manamgoda et al. 2012) by employing molecular tools. Usage of ITS (internal transcribed spacer), GPDH (glyceraldehyde-3-phosphate dehydrogenase; Fig. 1), LSU (large subunit) and EF1-α (translation elongation factor 1-α) or their combinations provided fine-tuning of the generic delimitation between the asexual stage of the genus Bipolaris and Curvularia and the sexual stage of the genus Cochliobolus (Manamgoda et al. 2012).

Fig. 1
figure 1

a Molecular phylogenetic analysis by maximum likelihood (ML) method based on the T92+G model substitution model (Nei and Kumar 2000) for the analysis of GDPH locus, and the generated have the highest log likelihood of −1093.94. The best substitution model parameters were determined based on Akaike information criterion, corrected (AICc = 2391.44), and Bayesian information criterion (BIC = 3147.14). The overall mean distance between taxa was 0.365 and the tree was rooted as previously described (Bengyella et al. 2014). The percentage of taxa that clustered together is shown next to the branches. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The evolutionary analyses were conducted in MEGA6 (Tamura et al. 2013). C. lunatus strains (DDBJ: AB859034, AB859035, AB859036, AB859037 and B859038) causing brown-to-black leaf spot disease of potato clustered together. Meanwhile, the 3 C. lunatus that clustered and are highlighted are clinical strains. b The image of Cochliobolus lunatus (GenbanK:JX907828) that causes disease of potato

Full size image

Combining morphological traits with GPDH improved differentiation of Cochliobolus species. We previously sequenced the GPDH locus of five virulent strains of C. lunatus causing brown-to-black leaf spot disease of potato (DNA Data Bank of Japan: AB859034, AB859035, AB859036, AB859037 and AB859038; Bengyella et al. 2014). The phylogenetic profile showed that economically important species such as the maize pathogen C. carbonum, and the oat pathogen C. victoriae are closely related, while the five strains of C. lunatus were sequenced form a group (Fig. 1). Although the five strains of C. lunatus clustered, they failed to cluster with other clinical strains of C. lunatus, signifying divergent evolution among the species. A direct consequence of this diversity is translated by the wide host range (Bengyella et al. 2014), diverse lifestyles and strategies for plant pathogenesis (Ohm et al. 2012). Whole genome sequencing of Cochliobolus species has revealed that C. lunatus is the most divergent species, considering only about 20% of its genome could align to the reference C. heterostrophus C5 genome, compared to about 75% alignment to other Cochliobolus species (Condon et al. 2014a, b; Liu et al. 2015).

Importantly, poor clustering could be cause by cross-mating of species as observed between C. carbonum and C. victoriae (Scheffer et al. 1967; Christiansen et al. 1998). Insights from analysis of C. heterostrophus revealed co-localization of effector genes and transposable elements (TEs), thus, exposing the effector genes to high rates of point mutations (Santana et al. 2014). Additionally, Santana et al. (2014) also identified that potential active TEs are found near coding regions and may modify the expression and structure of effector genes by acting as ectopic recombination sites. It is worth noting that introgression of TEs into genome could drive evolution since the activity of transposons and rearrangement sites can lead to a strong decrease in genome stability. Cross-mating and genome instability could cogently give rise to virulent resistance breaking pathotypes with wide host range (Table 1).

Table 1 Lifestyle of Cochliobolus species causing important economic loses
Full size table

Worldwide distribution of Cochliobolus species, risk of disease outbreaks and food security

To evaluate the distribution of Cochliobolus species worldwide and value regions likely to suffer from a disease outbreak, key words such as Curvularia, Cochliobolus and Bipolaris were queried in Google Scholar, NCBI, DDBJ and The Centre for Agriculture and Bioscience International (Cabi; http://www.cabi.org/isc/datasheet/14690), and the locations called up were computed using Google Maps tool (Fig. 2). Cochliobolus diseases are reported in wide geographical regions that include 26 Asian countries, 3 North American countries, 13 Central American countries, 10 South American countries, 11 Oceania countries and 8 European countries (CABI: http://www.cabi.org/isc/datasheet/14690). The spatial and temporal distribution indicated that 99 countries out of 196 countries on the globe have had at least a first report of disease caused by Cochliobolus species in sorghum, maize, wheat, rice and potato (Monteiro et al. 2003; Agrios 2005; Iftikhar et al. 2006; Louis et al. 2013). Zones where major epidemic of Cochliobolus diseases has not been reported is the Scandinavians were those where temperature on average is low (≤25 °C) throughout the year, suggesting higher temperature regions are more susceptible to Cochliobolus disease outbreaks. Nevertheless, Norwegian and Finnish barley production suffers from leaf spot disease and leaf blotch diseases of oat caused by C. sativus (Brodal et al. 2009; Ficke et al. 2011; Jalli 2011), indicating that Cochliobolus species gradually spread toward the Northern Hemisphere (Fig. 2).

Fig. 2
figure 2

Geographical distributions of Cochliobolus species and disease reports based on updated information in databases. Multiple pins indicate the region where Cochliobolus diseases have been reported several times. Selective mapping of important Cochliobolus species, e.g., ¥ indicates C. carbonum in barley and maize, \(\varPsi\) indicates C. heterostrophus in maize; dagger indicates C. lunatus in maize, rice, sorghum and wheat; filled triangle indicates C. miyabeanus in maize and rice; open square indicates C. sativus in rice and barley

Full size image

The uneven distribution of Cochliobolus species indicated that the Indian sub-continent and China are endemic zones (Fig. 3). It is worth noting that by 1987, Europe was free from Cochliobolus species (Sivanesan 1987). Geographically, Sivanesan (1987) noted that C. lunatus was predominant in Australia, Brazil, Guadalcanal, Guinea, India, Cameroon, Columbia, Ecuador, Fiji, Gambia, Malaysia, Nigeria, Pakistan, Papua New Guinea, Sierra Leone, Sri Lanka, Sudan, Tanzania, Thailand and the USA. By comparing the present data (Fig. 2) with that of Sivanesan (1987), it is revealed that Cochliobolus species have infiltrated into European countries such as Spain, the Netherlands, Italy, Hungary, Serbia, Cyprus, the UK and the Russian Federation in the last 29 years. This could pose an important challenge to farmers, since the crops grown in these regions might not have the necessary gene pool to mount effective resistance against Cochliobolus. As a result, increases in the likelihood of a disease outbreak could impact negatively on food security.

Fig. 3
figure 3

Cochliobolus species are widely distributed in the Indian sub-continent, China and the Pacific countries. Great epidemics such as the Northern leaf spot blight and corn head smut in Northern China in the 1990s (caused by C. lunatus and C. carbonum) and the Great Bengal rice famine (caused by C. miyabeanus) in the Indian sub-continent occurred in this region. Selective mapping of important Cochliobolus species, e.g., ¥ indicates C. carbonum in barley and maize; dagger indicates C. lunatus in maize, rice, sorghum and wheat; filled triangle indicates C. miyabeanus in maize and rice; and open square indicates C. sativus in rice and barley

Full size image

More revealing is the presence of Cochliobolus diseases in West Africa, viz., Cameroon, Nigeria, Niger, Benin, Sierra Leone, Ghana and Ivory Coast (http://maizedoctor.cimmyt.org/component/content/article/251-maydis-leaf-blight-extended-information; Jones and Jeutong 1993; Msikita et al. 2007; Fajemisin and Okuyemi 2009; Awoderu 2009), which are known to be heavy importers of rice from China and Thailand. Thus, it is tempting to hypothesize that Cochliobolus species may have been imported from Asia emanating from the Great Bengal rice famine in the 1940s and Northern leaf spot epidemic in Northern China in the 1990s. Given that Cameroon is largely considered as the bread basket of the Central African region, the chances that Cochliobolus species would spread to Chad, Central Africa Republic, Gabon, Equatorial Guinea and Congo are high. Previously, C. miyabeanus was reported to be responsible for 30–40% yield loss of maize in severe infections in Nigeria (Aluko 1975). Equally, 12–43% of yield loss in rice has been attributed to brown spot disease caused by C. miyabeanus in Nigeria (Awoderu 2009). On the other hand, yield loss of maize caused by C. heterostrophus estimated at 68% has been reported in the Western Highland of Cameroon (Ngoko et al. 2002). The high yield loss in Western Highland of Cameroon was associated with continuous cropping without a fallow period, decline in soil fertility and buildup of C. heterostrophus inoculum (Ngoko et al. 2002) and the unwillingness of farmers to use new varieties of maize. A serious issue that could arise is if the Cameroonian and Nigerian Cochliobolus species mate to produce aggressive progenies, keeping in mind the high volume of food trade between the two countries. In such a scenario, food security in the Central African region could greatly be affected. Hence, there is an urgent need to implement a coordinated local and cross-border/regional surveillance and control program for invasive Cochliobolus species.

Lifestyle variability of Cochliobolus species and management challenges

Even though Cochliobolus species lastly shared a common ancestor with other Dothideomycetes about 20 million years ago (Ohm et al. 2012), comparative genome analysis revealed divergent evolution reflected in their diverse lifestyles (Table 1) and hallmarked by different metabolic enzymes such as peptidase, lipase, glycoside hydrolase CAZymes, transmembrane domain protein, small secreted proteins and candidate effectors. Often, Cochliobolus species overwinters as mycelium in infected plant debris above the soil surface between planting seasons as saprophytes. Under favorable conditions of temperature and humidity at the onset of the planting season, mycelium grows and sporulates producing enormous inoculum (Jennings and Ullstrup 1957; Louis et al. 2015). Like other fungal pathogens, conidia are easily dispersed by wind colonizing subsequent hosts. Overwintering and huge inoculum could reduce the usefulness of dominant resistance plants (Melloy et al. 2010). The consequence of this life style results in increased cost of management in the bioeconomy. Irrespective of the pathogenesis of Cochliobolus species, C. lunatus, C. clavata and Cochliobolus spicifer are used as biocontrol agents (Abbas et al. 1995; Temur et al. 2014; Haroun et al. 2015) as an alternative to synthetic glyphosate derivatives. Although Cochliobolus species effectively control weeds in some cases (Temur et al. 2014; Haroun et al. 2015), their use as biocontrol agents complicate the management of disease in important crops.

Like other fungal pathogens, Cochliobolus species while in seeds remain dormant, but are actively transmitted to seedlings and mature plants which typically show symptoms such as reduced seed germination, radicle and plumule length and causes low vigor index as observed in fenugreek (Trigogella foenum-graecum) seeds (Khasanov et al. 1990). In recent years, it has been shown that Cochliobolus species causes diseases in several plant families including Alliaceae, Anacardiaceae, Araceae, Euphorbiaceae, Fabaceae, Malvaceae, Rutaceae, Zingiberaceae and Solanaceae (Manamgoda et al. 2011; Bengyella et al. 2014). Most Cochliobolus species are necrotrophs (Table 1) and invade their hosts superficially and subcutaneously, just below the epidermal layer, and occasionally produce appressorial-like structures (Brecht et al. 2007; Louis et al. 2015). Necrotroph of this nature could be difficult to control with synthetic fungicides because they must act superficially and be systemically absorbed. Additionally, given most necrotrophic pathogens have broad host range; they do not follow the gene-to-gene specificity when the host contains a dominant resistant gene. Consequently, controlling typical necrotrophic fungi requires multi-stacking of resistance genes or defense mechanisms to subdue disease severity (Chakraborty and Newton 2011).

Cochliobolus toxins enhances pathogenicity and disease burden

Comparative genome analysis indicated that when secondary metabolite genes are unique to Cochliobolus species or strain, they are likely to encode a virulent determinant (Condon et al. 2013). A historic Cochliobolus host selective toxin (HST) is T-Toxin, a polyketide toxin (Horwitz et al. 2013), produced by C. heterostrophus in Southern corn leaf blight (SCLB) epidemic. The T-toxin gene expression is modulated via G-protein and mitogen-activated protein kinase (MAPK) pathways (Degani 2015). Isolates of C. heterostrophus not producing T-toxin are call race O, but often produce small necrotic lesions on different cultivars of maize (Carson 1998). On the other hand, T-toxin producing strains produce chlorotic streaking and large necrotic lesions on Texas-type male sterile cytoplasm (cmsT) maize cultivars. Notably, race T is genetically unique from race O in that it has an extra 1.2 Mb DNA (Tzeng et al. 1992; Kodama et al. 1999), responsible for the production of HST. The interaction of URF13 protein (~13 kDa; unique to inner mitochondrial membrane) of cmsT maize with T-toxin heightens sensitivity and enhances virulence of the C. heterostrophus race T (Levings 1990; Dewey et al. 1987; Wise et al. 1987). URF13 protein has been shown to be a product of a new gene (T-urf13) that emerged from the recombination of mitochondrial DNA encompassing the ATPase gene promoter for subunit 6 and linked with the 26S rRNA gene and other sequences of unknown sources (Dewey et al. 1987; Wise et al. 1987; Levings 1990). The SCLB epidemic was effectively stopped in the late 1970s in the USA by introducing non-cmsT maize. Because of the good agronomic traits of cmsT maize, such as low cost, less labor involved in farming and no necessity to be detasseled to prevent self-pollination since it is sterile, it is preferred by breeders for producing hybrid seeds. As a result, worldwide replacement of cmsT maize has not been observed, making maize still vulnerable to C. heterostrophus race T. Significant progress led to the identification of two proteins Chlae1 and ChVel1 in C. heterostrophus race T that positively regulate T-toxin biosynthesis, pathogenicity and supervirulence, oxidative stress responses, sexual development and aerial hyphal growth, and negatively control melanin biosynthesis and asexual differentiation (Wu et al. 2012). Equally, C. heterostrophus produces another HST called ToxA-like protein, a virulence factor that induces light-dependent leaf necrosis of maize (Lu et al. 2015). Consequently, replacement of cmsT maize cultivars still exposes non-cmsT maize to C. heterostrophus ToxA-like protein and reduces maize yield.

The fungus C. carbonum race 1 produces a potent cyclic tetrapeptide (d-Pro-l-Ala-d-Ala-l-Aeo; Aeo stands for 2-amino-9,10-epoxi-8-oxodecanoic acid) referred to as HC-toxin which is a determinant of specificity and virulence during maize invasion (Walton 2006). The HC-toxin inhibits histone deactylases (HDACs). However, the impact of C. carbonum HC-toxin can be averted by maize carrying Hm1/Hm2 loci encoding for carbonyl reductase that detoxifies the toxin (Panaccione et al. 1992).

The fungus C. victoriae gained prominence during the 1940s Victoria blight of oats in the USA (Meehan and Murphy 1946; Macko et al. 1985) and the pathogen is highly virulent to oat carrying the dominant Vb allele (Litzenberger 1949). C. victoriae produces a cyclic pentapeptide HST called victorin that induces programmed cell death, and alone victorin is capable of causing disease without the fungus (Lorang et al. 2004). Buffelgrass (Cenchrus ciliaris) is an economically important pasture grass native to Africa and Southern Asia (Bogdan 1977). Buffelgrass is highly invasive and significantly damages the ecological dynamics of farmlands (Abella et al. 2012). A new metabolite named cochliotoxin produced by Cochliobolus australiensis has been shown to be phytotoxic to buffelgrass (Masi et al. 2017). Although C. australiensis reduces the quality of pasture grass, cochliotoxin (and C. australiensis) could be applied as biological control agents (Masi et al. 2017) in crop land invaded by buffelgrass.

The fungus C. miyabeanus generally causes brown spot disease of rice. Interestingly, the culture filtrate was found to suppress the production of phenol in planta (Vidhyasekaran et al. 1992). With the available new technologies such as ultrahigh-performance liquid chromatography (UHPLC) coupled to high-resolution Orbitrap mass spectrometry (HRMS), an aggressive strain of C. miyabeanus was found to produce tentoxin, a virulent factor required for symptom development during infection of rice (De Bruyne et al. 2016). Equally, non-ribosomal protein synthase (NRPS) CmNps3 was identified as a key enzyme in the biosynthesis of tentoxin (De Bruyne et al. 2016).

Besides HST, Cochliobolus species also produces non-HSTs previously reviewed in Stergiopoulos et al. (2012) that affect crop production, food quality or animal health. For instance, oosporein toxin inhibits ATPase activity, promotes cell lysis (Jeffs and Khachatourians 1997) and displays toxic effects on kidney and spleen at the range of 20–200 μM (Ramesha et al. 2015). The oosporein is often produced by fungus Cochliobolus kusanoi, a worldwide contaminant of maize, wheat and other cereals and adversely impact on food crops security and nutrition safety (Manning and Wyatt 1984).

Genomics evidence of evolving pathogenicity and epidemics

Variations in small cysteine-rich proteins (SCRPs) have been observed across the genus Cochliobolus based on genome-wide predictive studies (Condon et al. 2014a, b; Gao et al. 2014). The key roles played by SCRPs include induction of host hypersensitive reaction (van-den-Burg et al. 2003; Westerink et al. 2004), disruption of host recognition of pathogen or suppression of pathogen-associated molecular pattern (PAMP)-triggered immunity (Van-den-Burg et al. 2003; Dean et al. 2005). In Cochliobolus, key pathogenic factors such as toxin, melanin, cell wall degrading enzymes (pectinase, cellulase, hemicellulase, protease, amylase and phospholipase) and cutinase are essential for colonizing putative hosts (Nawas et al. 2017). Genome-wide analysis revealed that the number of these pathogenic factors varies between species such as C. lunatus CX-3 and C. heterostrophus C5 and between strains such as C. lunatus CX-3 and C. lunatus M118 (Gao et al. 2014). Equally, predictions revealed genome size variations (C. lunatus CX-3: 35.5 Mb; C. lunata m118: 31.2 Mb; C. heterostrophus C5: 36.5 Mb) and variations in protein-coding genes (C. lunatus CX-3: 11,234; C. lunata m118: 11,004; C. heterostrophus C5: 13,316) (Condon et al. 2014a, b; Gao et al. 2014).

Cochliobolus species are endowed with a high degree of genome plasticity (Condon et al. 2014a, b) that enhances their ability to evolve to highly virulent strains. For instance, genomic islands (GI) are composed of at least three contiguous genes encoding proteins (Fedorova et al. 2014) and are variably found in Cochliobolus genomes (Gao et al. 2014). Interestingly, C. lunatus CX-3 has 40 GI, whereas it is predicted that 16 GI separates C. lunatus m118 from the reference C. heterostrophus C5 (Gao et al. 2014). Some GI contain antibiotic resistance genes and GI often play key roles in symbiosis and pathogenesis, and enable microorganisms to adapt (Fedorova et al. 2014). Overall, this shows that different Cochliobolus species and strain variations in pathogenicity traits could be challenging to control in farms by a single approach, thus, hampering food production at different magnitudes.

Post-genomic era pathogenicity studies of Cochliobolus species relied on high throughput functional proteomics tools (Xu et al. 2007; Huang et al. 2009; Gao et al. 2012; Louis et al. 2014, 2016). Proteome analysis of C. lunatus interaction with maize led to the identification of proteins associated with photosynthesis, respiration, oxidative and drought tolerance and signal transduction (Huang et al. 2009), but no important defense genes were identified. Plant non-expresser of pathogenesis-related gene 1 (NPR1) is a vital gene involved in the regulation of plant defense (Dong 2004; Louis et al. 2016). Typically, NPR1 regulates the expression of pathogenesis-related protein (PR) gene expression through interaction with TGA transcription factors. Recent proteomics analysis showed that C. lunatus transiently down-regulates the expression of NPR1 at the onset of infection of potato and negatively affects photosynthetic and light assimilation pathways (Louis et al., 2016). Overall, C. lunatus down-regulated the number of peptide spots from 307 at 24 h after inoculation (hai) to 97 peptide spots at 96 hai (Louis et al. 2016). It was suggested that C. lunatus limits food production by disrupting the process that leads to carbohydrate production (Louis et al. 2016).

Iron metabolism plays a determinant role in fungi pathogenicity, since iron can mediate the production of ROS that leads to cellular damage via Fenton reaction (Fenton 1894; Winterbourn 1995). Fungi have the capacity to take up iron in the form of free iron ions, low-affinity iron chelates, siderophore–iron chelates, transferrin, heme and hemoglobin (Philpott 2006). Successful fungal phytopathogens have evolved their mechanism to achieve balance iron acquisition, chelation, storage of iron and detoxification of the oxygen radical free ion in their microenvironment (Kaplan and Kaplan 2009). Two high-affinity iron acquisition mechanisms well established in fungal phytopathogens are: (1) reductive iron assimilation (RIA) and (2) siderophore assisted (Haas et al. 2008; Johnson 2008). Two genes, NPS2 and NPS6, identified in C. heterostrophus encode different non-ribosomal peptide synthetases responsible for biosynthesis of intra- and extracellular siderophores, respectively (Condon et al. 2014a, b). It was shown that deletion of NPS6 leads to the loss of extracellular siderophore biosynthesis, attenuation of virulence, hypersensitivity, oxidative and iron-depletion stress and reduced asexual sporulation (Condon et al. 2014a, b). On the other hand, deletion of NPS2 mutants produced defective sexual spore development when NPS2 was missing from both mating partners (Condon et al. 2014a, b). This study further showed that C. heterostrophus RIA involvement in iron metabolism and virulence was overshadowed by that of extracellular siderophores as a high-affinity iron acquisition mechanism (Condon et al. 2014a, b). Thus, C. heterostrophus has diversified mechanism to metabolize iron, which enhances its pathogenicity and allow it to easily evade host-inherent ROS-mediated defense.

The abilities of Cochliobolus species to produce HSTs is one of the main causes of devastating SCLB that led to destruction of 15–17% of all US maize crops (Ullstrup 1972). In contrast to C. heterostrophus which produces HSTs, C. lunatus which causes diseases of maize, wheat, barley, cassava, potato and sorghum have evolved to produce non-host-specific toxin (methyl 5-(hydroxymethyl)-furan-2-carboxylate; Liu et al. 2009) and melanin (Xu et al. 2007). Another archetypal impact of Cochliobolus disease on food security that reshaped the socioeconomic fabric is the Great Bengal famine that caused starvation, death and mass migration within the Indian sub-continent (Padmanabhan 1973a, b; Scheffer 1997). This prompted migration and starvation of people within the sub-continent of India. Evolved virulent strains of C. lunatus CX-3 were among the leading pathogens that caused tremendous yield loss of maize in 11 provinces of maize cultivation in China in the early 1990s (Dai et al. 1995, 1998). In China, Northern corn leaf spot (NCLS) disease was first identified in 1972, and an outbreak in 1998 caused colossal yield losses ranging from 42 to 53% of all corn products (Liu and Wang 1999). It is worth noting that the epidemic in Northern China was severe, covering over 192,000 ha m2, resulting in the loss of 8 million kg yield in Liaoning province in 1996 (Dai et al. 1995, 1998). Supposing an average of 4 million kg yield loss was recorded in the 11 maize-producing provinces, this further implies that a gigantic total of 44 million kilogram yield loss could be envisaged with dire socioeconomic effects.

Intertwined relationship between temperature fluctuations, Cochliobolus species and crop production

Some invasive phytopathogens are often strongly regionalized and distributed in function of their plant host, climate, latitude and socioeconomic factors (Bebber et al. 2014a, b). Nonetheless, any subset of phytopathogens making gain in a new terrain poses challenges in crop protection and food security (Bebber et al. 2014b). The hemibiotrophic or necrotrophic relationship with hosts is dependent on key environmental factors (such as high humidity, low rainfall and high temperatures) which render them very aggressive and successful colonizers (Bandyopadhyay et al. 1991; Dubin and van Ginkel 1991; Saari 1998; Sharma and Duveiller 2004; Louis et al. 2015).

It is predicted that a global temperature increase of 1–3 °C could potentially increase global food production, but any increase above 3 °C decreases global food production (Easterling et al. 2007). Equally, Porter et al. (2014) estimated that changes in climate already reduced global agricultural output by 1–5% per decade over the last 30 years. The severity of Cochliobolus diseases is directly related to humidity and temperature (Acharya et al. 2011). Higher temperature (>25 °C) increases the virulence of C. lunatus on potato cultivars favoring subcutaneous and superficial colonization of leaves (Louis et al. 2015). Interestingly, it was found that when high temperature stress and wet climatic conditions were present, maize leaf spot disease was severe in maize fields (Gao et al. 2012). Most tropic and sub-tropic warm regions of the world such as Africa, Latin America, Asia and Southern Asia–Pacific where wheat and barley are cultivated suffered from high disease incidence caused by C. sativus (Dubin and van Ginkel 1991; Saari 1998; Sharma and Duveiller 2004). In these warm regions, head blight, seedling blight and spot blotch diseases of wheat caused by C. sativus have been reported (Zillinsky 1983; Wiese 1998). Temperatures between 18 and 32 °C favor the development of wheat-related Cochliobolus disease outbreaks, provided that the leaf remains wet for at least 18 h at a mean temperature ≥18 °C as in the case of Brazil (Reis 1991). On the other hand, a rapid and severe infection caused by C. sativus in India occurs at 28 °C than at lower temperatures (Singh et al. 1998; Acharya et al. 2011).

Thermotolerance experiments have shown that C. lunatus and Cochliobolus crepinii grow at 40 °C (Louis et al. 2015; Zhou et al. 2015). Extreme temperature fluctuations often threaten crop growth and development (Hatfield and Prueger 2015), alter conidia production (Louis et al. 2015) and may cause unpredictable turbulence in the interaction dynamics of Cochliobolus species with hosts. A study on weather variables (maximum and minimum temperatures, maximum relative humidity, total precipitation and frequency of precipitation) of mold development on sorghum grain over three consecutive seasons in South Africa (Tarekegn et al. 2006) led to the deduction that there is high correlation between the incidence of grain mold such as C. lunata, C. clavata, Alternaria alternata, Fusarium spp. (F. proliferatum and F. graminearum) and Drechslera sorghicola. These variations in climatic parameters impact negatively on the quantity, quality and value of food crops and enhance Cochliobolus diseases.

Intriguingly, it is known that C. heterostrophus causes significant yield losses in different maize cultivars from subtropical or temperate germplasm ranging from 9.7 to 11.7%, preferably under warm and humid conditions (Srivastava and Singh 2012). Atypically, how Cochliobolus species impact on food security largely depends on temperature, humidity, environmental survival of inoculum with novel traits, geography and transmission (Dubin and van Ginkel 1991; Saari 1998; Sharma and Duveiller 2004). It is accepted that man-made and natural risk factors and events, hallmarked by increasing temperature, is predicted to rise by 3.4 °C and CO2 concentration to increase to 1250 parts per million by ~2095 (Pachauri and Reisinger 2007). In this scenario of climatic condition fluctuations, Cochliobolus disease outbreaks are more likely to occur and compromise agriculture inputs and outputs linked with global food insecurity in major agricultural regions (Figs. 2, 3).

Blueprint to overcome Cochliobolus diseases and enhance food security

The growing human population and endless conflicts in some parts of the world coupled with dilapidated agricultural system compel us to produce more food to match global demand. Cochliobolus species complex biology and diversity in different or the same host at different geographical locations can produce variable symptoms (Bengyella et al. 2014) that are challenging to forecast, prevent or manage. For instance, in Uttar Pradesh, India, a new blight disease of C. lunatus characterized by elliptical brown spots on leaves, discolored glumes and discolored black kernel was reported (Simon and Lal 2013), contrary to brown leaf spots of rice in Punjab, Pakistan (Majeed et al. 2016) and in Cambodia (Tann and Soytong 2017) caused by C. lunatus. Hence, there is an urgent need of strengthening knowledge-based innovations, technology transfer, capacity development and training programs for farmers, students and researchers. Moreover, local and international decision-makers’ leadership and coordinated road-map policies, priorities and strategic interventions against Cochliobolus species threat on food security under the following guidelines are needed:

  1. 1.

    Improving early detection of invasive pathogens and recognition of symptoms for appropriate management: Farmers could benefit from training and empowerment programs which enables them to recognize earlier symptoms of Cochliobolus diseases under field conditions for appropriate rapid timely interventions and setting up of an integrated management strategy before epidemic breakout. Given farmers are the end users of research data, data sharing and supplying farmers and other agriculture stakeholders with free monographs of Cochliobolus symptoms on diverse crops would help in early detection of invaders and associated diseases. For a cohort of phytopathogens having important epidemic history, basic biology courses in schools should incorporate key features of Cochliobolus such as virulence, host-specific toxins, genome diversity and DNA finger printing techniques for species identification.

  2. 2.

    Strengthening knowledge-based information sharing and timely risk communication: Creating an open source knowledge sharing platform including social media networks with no monetary attachment, promoting first reports of Cochliobolus diseases in different regions with climatic conditions, identifying the species and accurate symptom description would help to check the migration of Cochliobolus species and could facilitate preparedness for any major threat or outbreak. Without an unbiased intelligence sharing platform and effective novel tools for all users and re-users on Cochliobolus species, food security conferred by rice, wheat, maize, sorghum, cassava and sugarcane would remain vulnerable. Consequently, the repeat of the Great Bengal famine could be envisaged in Africa, as Cochliobolus is gradually gaining terrain against crops of different gene pool (Fig. 2). Even though global quarantine could be considered, it would be ineffective given that plants, animals and humans seemless transmit Cochliobolus species (Bengyella et al. 2017).

  3. 3.

    Boosting awareness of the destructive potential of Cochliobolus species: Although Cochliobolus species were initially considered solely as plant pathogens, it is vital that the public be educated on their host range dynamics and their paradigm host jumping abilities. For instance, C. lunatus followed by C. geniculate, C. inaequalis and C. clavata infect animals and humans (Gugnani et al. 1990; Pimentel et al. 2005; Hay 2005; Bengyella et al. 2017), capable of causing ocular, respiratory and cerebral infections (Rinaldi et al. 1987). Given that Cochliobolus species interlocks with food security and human health, attention and funding injected into research on malaria, HIV/AIDs or other tropical diseases if supply in Cochliobolus disease research, it could ensure a universal durable plant protection strategy against Cochliobolus epidemics.

  4. 4.

    Nurturing intra- and intercountries research capacities: nurturing new research initiative and investment within and among poor countries with agriculture-driven economics could help ensure food security. Substantiating on this, predictive analysis on pathogen distribution showed countries with ability to monitor and efficiently report pathogen load increases with per capita gross domestic product, directly linked to the country research capabilities and expenditure (Bebber et al. 2014a, b, Bebber and Gurr 2015). Neighboring countries could strengthen phytosanitary testing system, establish standard seed testing protocols and collective surveillance and plant pathology research and development (R&D) in ensuring food security and sustainable development goals in Africa.

  5. 5.

    Developing and implementing new directives in fungicides and genetically modified crops: countries should invest in national/regional invasive species including Cochliobolus diseases R&D agenda in crops of interest to evidence-based agriculture policy decisions and priorities.

  6. 6.

    Enhancing stringent and robust screening of imported transgenic crops: often, transgenic crops are endowed with specific improved traits which are not directed toward controlling phytopathogens. Therefore, importing transgenic crops could introduce foreign dangerous microbes. For instance, between 2006 and 2013, the National Bureau of Plant Genetic Resources (NBPGR), New Delhi, India, screened a total of 4557 transgenic seed samples of various crops imported from different countries and intercepted Alternaria padwickii in rice, C. heterostrophus in maize, and C. miyabeanus and C. sativus in rice (Singh et al. 2014), indicating that surveillance and control interventions should be encouraged.

Outlook

Ever since the prediction that land degradation, urban expansion and conversion of crops and croplands for non-food production will decrease the total global cropping area by 8–20% by 2050 (Nellemman et al. 2009), there is an urgent need to understand how economically important invasive pathogens impact on food security. While food security entails safe food, quantity and appropriate nutrition, Cochliobolus species decrease farm yields, produce toxin in grains post-harvest and decrease quality. At present, there is lack of worldwide coordinated strategy for the management of Cochliobolus diseases despite the wide use of fungicides; thus, food security for subsistence farmers in developing countries is highly threatened. Because of the genetic diversity and complexity of most Cochliobolus genomes, core innovative biotechnology programs should be implemented in Nigeria, Cameroon, Benin, Ghana, Ivory Coast and Southern African region to monitor the evolution and migration of Cochliobolus diseases. To counter the threat posed by invasive Cochliobolus species in the context of global warming, polygenic resistance and heat adaptation traits, coupled with heterogeneous cropping, is preferable to help counter the virulence differential of Cochliobolus species. This could be a suitable pre-emptive control measure in African countries where Cochliobolus diseases are sparse (Fig. 2). Although C. lunatus has been used as a mycoherbicide for over two decades, and considering it is an airborne pathogen and exhibits diverse strategies to colonize new hosts (Louis et al. 2015), it would be prudent to restrict the use of C. lunatus as a biocontrol agent in the context of global climate change. This will help avoid introduction of laboratory mutant strains of Cochliobolus into the environment that could drive an arm race and trigger opportunistic expansion of the host range, rendering it ecologically unfriendly and negatively compromise on food security.