Maize Chlorotic Mottle Virus: Distribution, Alternative Hosts, Transmission Mechanisms and Management Options

Plant virus diseases are serious constraints to the productivity and profitability of a wide range of crops. Epidemics of existing plant virus diseases and the emergence of novel virus diseases have become a serious threat to subsistence and commercial agriculture. The knowledge of virus transmission and its survival helps to understand how the disease transmits from infected plant to healthy, where it reserved, and this will lead to identify the most important variables and focus efforts to develop sustainable management strategies. Maize chlorotic mottle virus (MCMV) is transmitted from location to location, and from plant to plant through various mechanisms (mechanically, seed, insect vectors, and soil) and many wild types of grass and cultivated crops, MCMV infected maize residue are used as its reservoirs. Different weed species and cultivated plants used as alternate hosts, and soil and seed transmissibility of MCMV are epidemiologically important and contribute to maintaining virus inoculum available in the absence of maize in the field and increase the chances of continuing its survival. Integrated disease management approach, regular field monitoring, assessment of virus symptoms, and rouging-out diseased plants are recommended to prevent further spread by insect vectors. Apart from this, because the disease is still widespread in various countries, intensive MCMV recruitment, combined with integrated disease management, requires ongoing practice in countries where MCMV is prevalent and in those countries that have not yet reported MCMV.


Introduction
Maize (Zea mays L.) is the main staple food in Latin America and Sub-Saharan Africa (Iken and Amusa, 2004). The crop is ranked the third most important cereal plant after wheat and rice (Khalili et al., 2013). Presently maize is cultivated throughout the year in almost every part of the world. The potential yield of maize per unit land area is highly dependent upon fertility levels, plant population, management practices, and the inherent potential of the variety adapted to that area.
Plant viruses are among the major factors that affecting food production worldwide and cause vast economic losses. It results in the loss by limiting plant produce quality and quantity (Thresh, 2006;Van der Vlugt, 2006) and have an estimated economic impact of more than $30 billion per year (Sastry and Zitter, 2014). Globally, there are more than 32 maize infecting viruses recorded on maize. Among them, Maize chlorotic mottle virus (MCMV) is one of the most devastating maize productions worldwide. Hence the objective of this paper is to overview the MCMV global distribution, host range, transmission mechanism, and its management options. mosaic virus (WSMV) (genus: Tritimovirus), their synergistic effect causes a more severe disease called Maize lethal necrosis (MLN), previously known as Corn Lethal Necrosis which leads to almost 100% field loss (Uyemoto et al. 1980;Goldberg and Brakke, 1987;Xie et al., 2011). When MCMV co-infects maize with any potyvirus infecting maize plants, a synergistic interaction occurs, causing a severe disease (Fig. 1) and yield losses. MCMV can cause 91% yield loss occurs in co-infection with either MDMV or Wheat streak mosaic virus (WSMV) (Niblett and Claflin, 1978). In Africa, MCMV is a serious disease of maize from its first outbreak in Kenya (Wangai et al., 2012) to the present (Regassa et al., 2020;. In Africa 30-100% loss in co-infection with SCMV (Wangai et al., 2012, Mahuku et al., 2015Guide et al., 2018;Regassa et al., 2020).

MCMV symptoms
Depending on the host genotype, MCMV infection symptoms range from mild to severe chlorotic mottle, leaf necrosis, stunted growth, a shortened male inflorescence with few spikes, malformed or partially filled ears, and premature death of plants (Niblett and Claflin, 1978;Uyemoto et al., 1981;Regassa et al., 2021).
When MCMV co-infects maize with a potyvirus infecting maize, the infected maize plants under field condition show a various range of symptoms, such as chlorotic mottling of the leaves (Fig 2 a and b), typically starting from the base of the young leaves in the whorl and extending upwards toward the leaf tips. The leaves can experience necrosis at the leaf margins that progress to the mid-rib resulting in drying of the whole leaf (Fig  2 d). Other symptoms include premature aging of the plants and mild to severe leaf mottling. Severely affected plants form small cobs with little or no grain set (Fig 2 f and g). The entire crop can frequently be killed before tasseling (Niblett and Claflin, 1978;Uyemoto et al., 1980Uyemoto et al., , 1981Wangai et al., 2012;Regassa et al., 2021).  Peru in 1973and reported in 1974(Castillo and Hebert, 1974 and thereafter was reported on maize plants in different countries of South America, North America, Europe, Asia and Africa. In Africa, MCMV was first occurred in Kenya in 2011 and reported in 202 (Wangai et al., 2012), since then have been reported and widespread in other East African countries. The following Table (Table 1) provides the year in which samples first tested positive for MCMV in each country it has reported in.  (Scheets, 2004), recent studies, however, have identified MCMV from sugarcane; finger millet, sorghum, Napier grass and Kikuyu grass (Wang et al., 2014;Kusia et al. 2015;Mahuku et al., 2015;Regassa et al., 2021). Our recent study (Regassa et al., 2021) showed that the Poaceae family had the highest number of grass species that were alternate hosts for MCMV, and Cyperus cyperoids and Cyperus cyperoides from the Cyperaceae family were naturally infected by MCMV (Regassa et al., 2021). Most of the natural alternative hosts identified were annual and perennial grasses in nature (Table 2), and common in the maize growing areas.  Regassa et al. (2021) Journal of Biology, Agriculture and Healthcare www.iiste.org ISSN 2224-3208 (Paper) ISSN 2225-093X (Online) Vol.11, No.19, 2021 22 Different types of MCMV symptoms were observed on different plant species of its alternative hosts. The symptoms observed included mosaics, mottling, yellowing, necrosis that develop from leaf margins to the midrib, and purple discoloration of leaves. For instance, MCMV symptoms on Cyperus cyperoids and Snowdenia polystachya were expressed as yellowing, while it showed mosaic and chlorotic symptoms on Oplismenus hirtellus (Fig.2) (Regassa et al., 2021). Bockelman et al. (1982) has identified a broad range of MCMV experimental host range that includes at least 19 grass species, but it does not infect dicots. According to Sheets (2004), 73 grass species in 35 genera have been tested for susceptibility to virus strains MCMV-Kansas, MCMV-Peru, or both (Table 3). Our recent MCMV experimental host range study (Regassa et al., 2021) revealed that among the 39 weed species tested for reaction to MCMV using artificial inoculation in the greenhouse, 20 species were susceptible to MCMV infection (Table 4). Cereal crops (barley and wheat) were also experimentally infected by MCMV (Fig 3, G and H).

Fig. 3. Maize chlorotic mottle virus (MCMV) on naturally infected different alternate hosts shows yellowing and mosaic symptoms. 2.4.2. Experimental host range
introduction of an infective virus or biologically active virus into a suitable site in the living cells through wounds or abrasions in the plant surface. Spreading viruses by the mechanical method is generally used for experimental purposes under laboratory/greenhouse conditions.

Insect vectors
The transmissions of viruses from plant to plant by vectors provide the main method of spread in the field for many viruses including MCMV that cause severe economic loss (Hull, 2014). In Ethiopia, studies on the MLN (MCMV is the main component) distribution and factors associated with its epidemic show that the spread of MLN causing viruses (MCMV and SCMV) are linked to the free movement of insect vector and continuous availability of the host plants (Regassa et al., 2020). In the United States mainland, MCMV has been reported to be transmitted by six different species of chrysomelid beetles, including the cereal leaf beetle (Oulema melanopa), corn flea beetle (Chaetocnema pulicaria), flea beetle (Systena frontalis), southern corn rootworm (Diabrotica undecimpunctata), western corn rootworm (Diabrotica virgifera) and northern corn rootworm (Diabrotica longicornis) (Jiang et al., 1992;Nault et al., 1978).
The other vector that transmits MCMV is maize/ corn thrips, Frankliniella williamsi Hood (Thysanoptera: Thripidae) has been identified to be the main vector (Cabanas et al., 2013) in Hawai, USA. Maize thrips transmit MCMV in a non-persistent manner. Both larvae and adults of corn thrips transmitted MCMV for up to 6 days after acquisition, with decreasing rates of transmission as time progressed.

Seed Transmission
MCMV is also transmitted by seed. The rate of MCMV seed transmission observed by Jensen et al. (1991) who evaluated 42,000 seedlings and found a 0.04% transmission rate in Hawaii, USA. In line with this finding Quito-Avila et al. (2016) from Ecuador reported 8 and 12% seed transmission of MCMV. Zhang et al. (2011) reported MCMV seed transmission of 2 seeds in 600 (0.33%) in Chinese maize. Our recent MCMV seed transmission study result (Regassa et al., 2021) showed the mean seed to the seedling transmission rate of MCMV was 0.073% with a range of 0 to 0.17% among 20 different maize varieties studied. Fourteen maize genotypes had some levels of seed transmission (0.03%-0.017%) for MCMV. Seed transmission rates of the viruses were influenced by the seed lot and maize varieties used.

Transmission through soil and plant residue
Transmission in soil water or crop residues has been suggested for MCMV, and there are a number of reports of increased disease pressure after heavy rainfall and in soils with a higher water capacity (Jensen, 1991;Uyemoto, 1983). Mahuku et al. (2015) found that planting clean seeds in the soil from MLN-affected areas resulted in 69% MCMV infection. Our current study also confirmed that low soil transmission (4.24-13.5%) MCMV can be transmitted from infested soil to newly raised maize seedlings and it also reserved in maize residues (Regassa et al., unpublished data). Similar findings were previously reported on MCMV transmission through soil (Nyvall, 1999). It also reported that MCMV can be transmitted through infected plant residues that play important roles in the survival of the virus especially when maize is planted during the off-season (Uyemto, 1983;Montenegro and Castillo, 1996).

Management of MCMV
Plant virus diseases including MCMV are intrinsically difficult to manage directly by measures such as direct use of chemical pesticides, an integrated management options which include the use of disease-resistant crop varieties, the uses of cultural practices like crop sanitation and removal of infection sources, use of virus-free seeds and chemical pesticides such as seed treatment and foliar spray to indirectly control vector insects is the most feasible option.
The most effective control for MCMV has been achieved through the integration of cultural practices with insecticides and host resistance (Nelson et al., 2011). Alternatively, crop rotation with non-maize crops has been shown to reduce the incidence of MCMV the following year (Phillips et al., 1982;Uyemoto, 1983). Maize Producers are advised to practice crop rotation for at least two seasons with alternative non-cereal crops such as potatoes, sweet potatoes, cassava, beans, bulb onions, spring onions, vegetables and garlic. Planting different crops each season will diversify farm enterprises. Manure and basal/top dressing fertilizers can be applied to boost plant vigor.
It is necessary to use good field sanitation methods, including weed control measures to eliminate alternate hosts for potential vectors (Wangai et al., 2012;Regassa et al., 2020Regassa et al., , 2021. Infected foliar material should be removed from the field to reduce pathogen and vector populations. In Hawaii, USA producers of maize seed spray regularly after planting to control insects that spread the virus (Nelson et al., 2011). The use of tolerant or resistant varieties ultimately would be the most effective means of managing MCMV (Regassa et al., 2020). Superior resistance to MCMV is widely available in tropical maize seed stocks and provides the best control for this disease. The use of host resistance is the most desirable and feasible method in virus disease management. According to Nelson et al. (2011), trials performed in Hawaii in 2011 found many tropical inbred lines and varieties to be highly resistant to MCMV. Almost all temperate climate inbred lines and hybrids are highly