Southern corn rust caused by Puccinia polysora Underw: a review

Abstract

Southern corn rust (SCR) caused by Puccinia polysora Underw is one of the most devastating maize diseases, resulting in substantial yield losses worldwide. The pathogen is an obligate biotrophic parasite that is difficult to culture on artificial media. In recent years, the disease has become prevalent—both globally and in China—and increasing difficult to control because of its wide distribution, long-distance migration, multiple physiological races and fast evolution, all of which have contributed to a considerable increase in the risks of associated epidemics. In this review, we summarize the current knowledge of P. polysora, with emphasis on its global distribution (particularly in China), life and disease cycle, population genetics, migration, physiological races, resistance genes in maize and management. Understanding the underlying factors and processes in SCR epidemics should facilitate management of the disease and breeding for resistant maize varieties.

Background

Maize (Zea mays L.) is the most highly produced and economically important cereal crop globally. Owing to an increase in demand for maize in China, its production has surpassed by far those of rice and wheat (Wang et al. 2019). In 2019, the world’s total yield of maize was 1,148 million tons, whereas rice and wheat yields were only 755 million and 766 million tons, respectively (FAO 2019). However, the annual yield loss attributed to southern corn rust (SCR) has significantly increased because of the lack of maize varieties with a high degree of resistance to SCR (Futrell et al. 1975; Brewbaker et al. 2011; Liu et al. 2016). Consequently, SCR poses a great threat to global maize production and, therefore, to global food security. In this review, we focus on the symptoms of SCR and the biological characteristics of the pathogen causing this disease, its distribution and migration trends, physiological races, resistance genes in maize and disease management. In general, our review aims to enhance our understanding and management of SCR.

Global distribution of SCR

Puccinia polysora, the causal agent of SCR, was first described and named by Underwood in 1897 (Underwood 1897), after it was first identified in 1891 on a herbarium specimen of eastern grama grass (Tripsacum dactyloides L.) in Alabama, USA (Underwood 1897). However, in 1879, Cummins had observed that SCR was widespread in Central and South America as well as in Massachusetts, USA, i.e., much earlier than the reported identification in 1891 (Krattiger et al. 1998). The pathogen shows enormous destructive potential in maize (Melching 1975). It was later reported that the pathogen can infect teosintes, including two Erianthus species and four Tripsacum species (Cammack 1959a). However, in early days, the role of P. polysora in epidemiology was unknown.

In 1949 and 1950, for the first time, SCR epidemics were reported in Sierra Leone, Liberia, Ivory Coast, Gold Coast, Dahomey, Togoland and Nigeria in West Africa, resulting in yield losses of up to 50% (Rhind et al. 1952). By 1952, SCR had reached Tanganyika, Uganda, Nyasaland and Kenya, and the east coast of Africa including the Republic of Mauritius which is in the Indian Ocean and is the most eastern point of disease migration, thereby posing a threat to maize production in Asia and Australia (Orian 1954); it was also reported in Canada in 1954 (Orian 1954). In 1953, it caused 80–84% yield losses in the Philippines (Reyes 1953). SCR was first noticed in south India in October 1957, with a mild infection in maize (Payak 1992). In 1959, SCR infestations were observed in Australia (Barker 1969). SCR emerged in Thailand in 1967 (Brewbaker et al. 2011). At the same year, the first authentic specimen of the disease was found in Hawaii (Raabe et al. 1981). In the 1900s, disease surveys carried out by the Brazilian Agricultural Research Corporation (Embrapa) revealed that SCR was one of the most important maize diseases and caused 40% losses in susceptible maize varieties (Bulow 1966; Krattiger et al. 1998). The epiphytotic of SCR extended to the main part of the maize belt in the United States during 1972–1974, causing 30%–50% yield losses (Futrell et al. 1975). By 1997, SCR had also become widespread in the Okinawa, Kyushu, Shikoku and Yamaguchiken prefectures of Japan (Hirayae et al. 1998). In addition, in 1951, a disease similar to SCR was described in Kumamoto, Japan (Nishi et al. 1998). In China, the disease was first identified in Hainan Province in 1972 (Duan and He 1984). According to an SCR distribution map published by the Center for Agriculture and Bioscience International (CABI), the disease has been found in more than 110 countries spanning Africa, Asia, the Americas and Australasia (CABI 2021; Fig. 1).

Fig. 1

Worldwide distribution of southern corn rust. The red areas represent the occurrence regions of southern corn rust (CABI 2021)

Temperature and humidity are the main factors influencing cereal rust spore germination, penetration, establishment and spread (Pavgi 1972). Potential future distribution of SCR was modeled using the CLIMEX software based on current geographic locations and temperature and humidity conditions. According to the results, SCR occurs in all continents; furthermore, future trends might incline towards a general reduction in incidence in the Southern Hemisphere concomitant with general increase in incidence in the Northern Hemisphere (Ramirez-Cabral et al. 2017).

SCR in China

In China, maize is widely cultivated in areas ranging from eastern coastal provinces to western provinces and from Hainan Province in the south to Heilongjiang Province in the north (Guo 2010). The area under maize cultivation in China can be divided into six regions (spring maize in the northeast area, summer maize in the Huanghuaihai area, southwestern mountainous area, southeastern maize area, tropical area and subtropical area). To increase production, numerous high-yield varieties are bred, such as Zhengdan 958, Xundan 20 and Xianyu 335, which have become the main cultivated corn varieties in China; however, all these three varieties are susceptible to SCR (Liu et al. 2009). Indeed, Wang et al. (2006) investigated the resistance of 178 corn varieties to SCR, and reported that only 25(14%) varieties were highly resistant or resistant to SCR, whereas the majority (86%) were susceptible. In 1998, the disease outbroke in Hebei, Jiangsu, Shandong and Henan provinces. This was the first report of the disease in the northern areas of China since it was first identified in Hainan Province in 1972 (Duan and He 1984; Liu et al. 1998). At present, SCR has become a serious disease in more than 20 provinces/cities, including Hainan, Guangdong, Guangxi, Fujian, Jiangxi, Hunan, Guizhou, Yunnan, Chongqing, Hubei, Zhejiang, Anhui, Jiangsu, Henan, Shannxi, Shanxi, Shanghai, Shandong, Hebei, Tianjin, Beijing and Liaoning (Fig. 2). In our surveys, we observed that SCR occurred earlier in southern areas than in northern areas (unpublished data). Typhoons can efficiently enhance long-distance spore dispersal of P. polysora, and the landing pathway and duration of typhoon will determine the range and severity of SCR (Wang et al. 2020a). Owing to the cultivation of susceptible varieties over large areas and a favorable climate for disease development, SCR displays an aggravating tendency in China (Liu et al. 2018). In 2015, the affected area and yield losses caused by SCR were 5.289 million hm² and 756 million kg, respectively, which were 4.5-fold and 8.8-fold great than the annual averages of 2008–2014 (Liu et al. 2016; Fig. 3).

Fig. 2

The distribution of Puccinia polysora and the possible resources of primary infection of P. polysora causing southern corn rust in China. Broken black arrows indicate the possible pathway of urediniospores dispersed by the wind (Liu et al. 2018; Wang et al. 2020a)

Fig. 3

The occurrence area and prevention area of southern corn rust, and actual losses and recover losses of maize in China during 2008–2015 (Liu et al. 2016)

Symptoms and biological characteristics

P. polysora is an obligate parasite that infects, grows and reproduces only on living maize plant tissues (Unartngam et al. 2011). The pathogen infects all the aboveground parts of maize plants including leaves, sheaths and stems (Fig. 4). Its damage is considerably more devastating and lethal than common rust damage caused by Puccinia sorghi Schw. (Scott et al. 1984). Pustules of P. polysora are primarily produced on the upper leaf surfaces, distinguishing them from common rust whose pustules develop on both sides (Crouch and Szabo 2011). Urediniospores of SCR are one-celled, yellowish to golden, echinulate, with 4–5 equatorial pores; whereas teliospores are two-celled, chestnut brown, angular to ellipsoid or oblong (Krattiger et al. 1998). When urediniospores of these two fungi are treated with 95% sulfuric acid or 75% hydrochloric acid, the protoplast of P. polysora contracts into the shape of a ball but that of P. sorghi contracts to resemble several balls—a difference that can be used to distinguish between these two species (Huang et al. 2020). The sporulation of urediniospores from a single pustule could last 18–20 days, which can release 1,500–2,000 and 600–1,150 spores daily from susceptible and resistant plants, respectively (Cammack 1962). Teliospores are produced in the late season or not at all and are covered by the epidermis, rendering the observation more difficult (King and Scott 1982; Crouch and Szabo 2011).

Fig. 4

Southern corn rust symptoms. a Urediniums on adult maize plants. b Urediniums on the sheath. c Urediniums on the sheaths, bracts and stem. d A urediniospore under a scanning electron microscope (SEM). e Urediniums on a maize leaf. f A uredinium under a SEM

SCR thrives under high temperature and relative humidity (Shurtleff 1980). The optimal temperatures for the germination of urediniospores and disease development are 26–28 °C and 24–27 °C, respectively; the temperature range for disease occurrence and development is 15–31 °C (Yang et al. 2015). Li et al. (2019) reported that the density of urediniospores in the air was significantly and negatively correlated with temperatures above 27 °C and sunshine duration. Similarly, Godoy et al. (2003) found that the epidemic rate of SCR in Brazil was positively correlated with the mean daily temperature but negatively correlated with sunshine hours when relative humidity was > 90%. In addition, analysis of the biochemical parameters of the pathogen revealed that SCR is a high-sugar disease (Huang et al. 2012).

Life cycle and disease cycle

The life cycles of most cereal rusts are well understood (Jin et al. 2010). However, the life cycle of P. polysora remains unclear (Cammack 1959a; Guo et al. 2013). Teliospores are rarely produced in mature plants or not produced at all (Crouch and Szabo 2011), and are sometimes covered with an epidermis and do not dehisce, which makes it difficult to find them (Crouch and Szabo 2011). Series experiments to induce teliospore germination have been unsuccessful (Cammack 1962; Brewbaker et al. 2011). Therefore, the function of teliospores in the fungal life cycle is unclear, although teliospores might play a role in pathogen survival. Urediniospores serve as the primary inoculum sources for maize infection, known as the mini cycle of P. polysora (Brewbaker et al. 2011), but the aecidial and pycnidial stages of P. polysora remain unknown (Cammack 1959a).

In China, SCR can occur in most summer maize areas where ambient temperature favors the disease development. We found that the causing pathogen, P. polysora, can overwinter and survive throughout the year with a continuity of the uredo-stage in the southern areas of China, where maize can be planted throughout the year (Fig. 5). The wind transports urediniospores from such southern areas to the major summer maize-producing area in the Huanghuaihai region of China, where the pathogen cannot overwinter.

Fig. 5

Disease cycle of southern corn rust in China. Two types of disease symptoms were observed on maize, the uredinial stage with corresponding urediniospores and the telial stage with teliospores (Crouch and Szabo 2011). The disease symptoms at the basidial, pycnial and aecial stages appearing on an alternate host are unknown. The pathogen can survive and repeat its asexual cycle by urediniospores throughout the year in south. In summer, the wind transports urediniospores from south to north where the pathogen cannot over-winter

Population genetics

General knowledge regarding the levels of genetic diversity in P. polysora populations remains limited. In Japan, at least two genetic groups were found based on genetic diversity analysis of 14 isolates using restricted fragment length polymorphisms (RFLP) of the internal transcribed spacer 1 (ITS1) and ITS2 regions (Hirayae et al. 1998). Similarly, in Thailand, Unartngam et al. (2011) divided 38 specimens from different provinces into 13 groups at 75% Dice’s similarity coefficient based on the results of genetic diversity analyses of P. polysora using five inter-simple sequence repeat (ISSR) markers. They found that isolates from different provinces were presented in the same group and those from each province were clustered into more than one group, indicating that the genetic diversity of the isolates has no correlation with their geographical distribution. In turn, in China, the similarity of the ITS and β-tubulin sequences of the isolates sampled in Hainan, Henan and Chongqing was 99.12%–100% and 98.97%–99.91%, respectively (Xing 2011). However, in another study, a total of 72 isolates collected from 12 provinces in China were clustered into 2 groups and 5 subgroups of 10 branches, with high genetic diversity, based on 18 polymorphic ISSR primers (Guo et al. 2013). The results showed that all the isolates collected in 2011 and eight isolates collected in 2012 were clustered in one group, but the other isolates collected in 2012 were clustered in another group, suggesting some relationships in the subgroup population based on collected loci and years.

P. polysora migration

P. polysora urediniospores can be dispersed by wind currents to elevations higher than 15,000 ft and over long distance (Orian 1954). Cammack (1958) identified two main size groups of urediniospore—namely, a small size group in Southeast Asia and neighboring islands and a larger-size group in the West Indies, Africa and the South Indian Ocean—consisting with two directions (eastwards and westwards) of migration from their origin in the region of the Caribbean. However, the examination lacked data on cross-inoculation studies, which indicated that it is uncertain if distinct forms of P. polysora exist. Cammack (1959b) speculated that urediniospores were the only source of infection dispersing from the Caribbean to Africa. In Thailand, specimens collected from different provinces were clustered in the same group because of urediniospore migration (Unartngam et al. 2011).

In China, no significant sub-population differentiation has been found among Hainan, Henan and Chongqing, implying potential frequent gene flows among these places (Xing 2011). However, Guo et al. (2013) reported low gene flows among provincial populations, and the pathogens in Hainan, Guangdong and Guangxi were not the original sources of the disease in summer maize in the Huanghuaihai area, indicating that the pathogen in China may originate from other areas outside the mainland of China. Conversely, Liu et al. (2018) inferred that P. polysora emergence in Tianjin was likely attributable to long-distance wind dispersal from southern China. In addition, according to Wang et al. (2020a), Taiwan, China, is the original source of the pathogen found in the Huanghuaihai region, and Liaoning, Zhejiang, Fujian, and Guangdong provinces; the Philippines is the source of the pathogen in Guangdong, Guangxi and Hainan; and Thailand and other neighboring countries are the sources of the pathogen occurring in Yunnan and Guizhou provinces (Fig. 2). Based on the previous studies and our surveys of P. polysora, we inferred that the pathogen in the southern area in China where the disease can over-winter could be the source of SCR occurred in summer maize in the Huanghuaihai area of China (Liu et al. 2018; Wang et al. 2020a; Fig. 2).

Physiological races

Several physiological races of P. polysora have been identified. In 1952, EA1, the first physiological race of P. polysora, was recognized from urediniospore collections sampled in Zanzibar, Tanganyika and Uganda (Storey and Howland 1957). The EA2 race was subsequently identified in Zanzibar, Northern Tanganyika and Uganda using four maize lines in 1955 (Ryland and Storey 1955), whereas the EA3 race was found in Kenya in 1961 (Storey and Howland 1967a). Six novel physiological races, PP.3, PP.4, PP.5, PP.6, PP.7 and PP.8, distinct from the East African races, were identified in Georgia, Nicaragua, Colombia, Mexico, Florida, Nicaragua and Puerto Rico of North and Central America, using 11 maize cultivars as differentials (Robert 1962). The tenth race, PP.9, was identified in South Africa in 1965 (Ullstrup 1965). In Brazil, 17 virulence patterns were identified in 60 single pustule isolates using six maize cultivars (Casela and Ferreira 2002). SCR occurs globally; however, race identification of P. polysora has been performed using maize differentials with different genetic sources (Storey and Howland 1957; Robert 1962; Ullstrup 1965; Casela and Ferreira 2002). Owing to the lack of unique differentials and a high variability of the causing pathogen, the identification and application of resistant genes against SCR in maize plants have been limited. Further, in tropical regions, the constant failure of studies on race-specific resistance to SCR has been attributed to the occurrence of multiple races of the pathogen in tropical areas (Casela and Ferreira 2002). According to Keller et al. (2001), race-specific resistance is ineffective, unstable and short-lived owing to the rapid evolution of the pathogen. Therefore, there is an urgent need to identify and classify the physiological races and virulence patterns of P. polysora.

SCR-resistant genes

The identification of resistance genes can facilitate maize breeding and production programs (Babu et al. 2004). The identification of SCR-resistant genes began as early as the 1950s. In 1957, Rpp1 and Rpp2, two genes conferring resistance to two physiological races of P. polysora EA1 and EA2 were identified from AFRO.29 (Colombia 2) and AFRO.24 (SLP 20-4A) maize lines originating in Columbia and Mexico, respectively (Storey and Howland 1957, 1959). Rpp1 is completely dominant and confers high resistance to EA1, but not to EA2, conversely, Rpp2 is incompletely dominant and confers equal resistance to these two races (Storey and Howland 1957). In addition, neither Rpp1 nor Rpp2 exhibited resistance to EA3. Backcross segregation, repulsion and coupling studies on seedlings inoculated with EA1 and EA2 revealed that Rpp1 and Rpp2 are linked, with an estimated recombination rate of 12.23% (Storey and Howland 1959). Rpp3–Rpp8 were identified by Robert (1962) using a series of maize lines. Rpp9, which is closely linked to Rpp1, was from PT186208, with resistance to the PP.9 race isolated in Indiana (Scheffer and Ullstrup 1965). Rpp10 and Rpp11 were isolated from AFRO.761 (Andaqui, Colombia) and AFRO.600 (Zapalote Chico, Mexico) maize lines, respectively, of which Rpp10 is fully dominant and exhibited high resistance to both EA1 and EA3, whereas Rpp11 is incompletely dominant and exhibited incomplete resistance to EA1 and EA3 (Storey and Howland 1967b).

Recently, numerous studies have shown that major quantitative trait loci (QTL) and SCR resistant genes are mapped to the short arm of chromosome 10 (Table 1) (Liu et al. 2003; Chen et al. 2004; Zhang et al. 2009; Yao et al. 2013; Zhang 2013; Wu et al. 2015; Wang et al. 2020b; Meng et al. 2021). Effective identification of the loci for SCR resistance-related genes will facilitate the breeding of SCR-resistant maize varieties. RppP25, a major resistance gene from the inbred maize line P25 (China) was roughly mapped on chromosome 10S with a 5.8 cM genetic distance from the simple sequence repeat (SSR) marker phi059 (Liu et al. 2003). In addition, a single dominant gene, RppQ, was identified from the Qi319 (China) maize line, and was mapped on the short arm of chromosome 10S between the SCAR marker MA7 and the AFLP marker M-CCG/E-AGA157 with a genetic distance of 0.46 and 1.71 cM, respectively. (Chen et al. 2004; Zhou et al. 2007). Additionally, genetic analysis revealed that the resistance of the inbred line W2D (China) was controlled by a dominant RppD, which was mapped on the short arm of chromosome 10S flanked by the SSR marker UMC1291 and the CAPS marker CAPS858 with a genetic distance of 2.9 and 0.8 cM, respectively (Zhang et al. 2009). Furthermore, in the inbred line CML470 developed by CIMMYT, a dominant RppC was identified, which was mapped on the short arm of chromosome 10S in the region between the SSR markers UMC1380 and UMC1291 with a genetic distance of 3.5 and 8.8 cM, respectively. (Yao et al. 2013). Similarly, the Jiku12 (China) resistance gene was identified as a dominant Rpp12 distinct from RppQ and mapped on the chromosome 10S with a genetic distance of 4.2 cM away from the adjacent molecular marker PHI063 (Zhang 2013). In turn, the tropical inbred line SCML205 (China), harbors a single dominant resistance gene, Rpps, which was mapped on the distal arm of chromosome 10S (Wu et al. 2015). In addition, Wang et al. (2020b) identified and mapped a resistance gene, RppM, from the near-isogenic line Kangxiujing2416 (Jing2416K) to a 3.69 Mb region on chromosome 10S, and the RppCML496 resistance gene was detected in CML496 (CIMMYT) and delimited to a 128 kb interval on chromosome 10 (Meng et al. 2021). Furthermore, two major resistance QTLs, qSCR6.01 and qSCR10.01, were identified from the Qi319 (China) maize line (Lu et al. 2020). Particularly, unlike the previous identified major genes/QTLs for SCR resistance on chromosome 10, qSCR6.01 is the first identified major QTL associated with resistance to SCR on chromosome 6.

Table 1 Summary of SCR-resistant genes

In addition to the major genes/QTLs abovementioned, QTLs with partial resistance to SCR have been reported based on linkage or association mapping, which offer additional genetic resources and information essential for maize breeding (Chen et al. 2019; Deng et al. 2019; Meng et al. 2021). For example, using recombinant inbred lines derived from a cross between Ye 478 and Qi319, Lu et al. (2020) identified three QTLs designated as qSCR3.04, qSCR5.07 and qSCR9.03 on chromosomes 3, 5 and 9, respectively, which effectively explained 2.84% to 3.11% of the total phenotypic variation in each QTL. In addition, Deng et al. (2020) reported a major QTL named Ascr4.01 on chromosome 4, which can explain 48% to 65% of the total phenotypic variation, based on a recombinant inbred line derived from a cross between CIMBL83 and Lx9801. QTLs with minor effects or partial resistance to SCR have been detected on all maize chromosomes, which provide more valuable source for SCR resistance (Brewbaker et al. 2011; Wanlayaporn et al. 2013; Zhou et al. 2018; de Souza Camacho et al. 2019; Chen et al. 2019; Deng et al. 2019, 2020; Lu et al. 2020).

The resistance genes Rpp1–Rpp11 appear race-specific, whereas the other resistance genes exhibit complete resistance to SCR. The pathogen evolves rapidly, so that new race overcomes the resistance gene like Rpp9, which is used to breed resistant maize varieties in Southern US. These findings highlight the need for identifying novel resistance resources (Brewbaker et al. 2011).

Disease control and integrated management

The use of resistant crop varieties is considered an effective and environmentally friendly strategy for disease management. In China, several maize varieties, such as Nongda108, Zhengda619, Chengdan22 and Jundan20, have been identified to be resistant or highly resistant to SCR (Yuan et al. 2010). Intercropping can also reduce the severity of the disease. Liu et al. (2013) compared infection severity and defense-related enzyme activity in mono-cropping and inter-cropping systems inoculated with SCR, and according to the results, inter-cropping significantly enhanced defense and resistance to SCR.

Disease prediction models and monitoring networks are used as early warning systems in disease management schemes (Isard et al. 2011; Liu et al. 2015). Additionally, a molecular detection system for monitoring SCR has also been established (Leng et al. 2012), and spectral disease indices (SDIs)-based monitoring models have been developed for evaluating infected leaves and classifying the severity of SCR damage. Such models have provided a sound theoretical basis for remote sensing of SCR in the field (Meng et al. 2020). Additionally, a prediction model has been established for the prediction of SCR disease index (Li et al. 2019). Indeed, Spurlock et al. (2020) observed a significant positive correlation between relatively high normalized difference vegetation index (NDVI) and SCR severity based on remote sensing analysis, which facilitated the development of a more reliable SCR scouting model.

Chemical control is used in preventing the epidemic of plant diseases. Although, there is no SCR-specific fungicide, in the maize booting stage, 12.5% epoxiconazole SC effectively controlled SCR damage by up to 85.54%, which was only 20%–40% under conventional fungicides, such as triadimefon and zineb (Hu et al. 2003). However, Faske and Emerson (2021) found that the application of quinone outside inhibitor (Qol) or Qol + demethylation inhibitor (DMI) fungicides at tasseling stage were most effective when SCR was present and environmental conditions favored rust development. In addition, a combination of triazole and estrobirulina was feasible to reduce SCR severity (Moratelli et al. 2015).

Conclusions and future perspectives

SCR is a major maize disease reported globally. The wide occurrence of this disease and the resulting yield losses are causes for deep concern from all stakeholders, including researchers. The analysis of the biological characteristics, distribution, races and genetic structure of the causing pathogen, P. polysora, in various regions has offered key insights into its historical and contemporary emergence, revolution and also migration trends. Considering it is highly invasive and potentially catastrophic, globally concerted efforts are needed to prevent pathogen incidence and spread. In the past, physiological races of P. polysora were identified using maize differential lines. However, due to the loss of two maize lines, the classification of races was suspended (Guo et al. 2013), resulting in the discovery and mapping of resistant genes based on complete resistance to SCR rather than race-specific resistance. The establishment of a novel differential host system is required for the identification of new physiological races, evaluation of spatiotemporal dynamics of races, and cultivation of resistant varieties. Studies on P. polysora migration based on population genetics are scarce now. Furthermore, the lack of useful genetic markers for P. polysora impedes research on the migration of the disease. Nevertheless, the development of SSR and single nucleotide polymorphism (SNP) markers would facilitate an understanding of pathogen population diversity and migration. Integrated management strategies are required for SCR. Furthermore, a convenient, cost-effective, specific and rapid diagnostic tool for predicting and monitoring disease incidence should be developed. Currently, our understanding of the alternate host of P. polysora and the roles of teliospores in host–pathogen interactions is inadequate. Considering that mining resistance genes are critical for breeding SCR-resistant maize varieties, the maize germplasm available globally should be screened to identify novel SCR-resistant genetic sources.