Macrophomina phaseolina

An example of a pathogen with a very wide host range is Macrophomina phaseolina (Tassi) Goid. Macrophomina phaseolina has no known sexual stage. However, it is classed as an ascomycete based on the presence of DNA sequences for mating-type alleles (Nagel et al. 2018). It has been identified as the cause of charcoal rots in stem infections and damping off when roots are compromised for more than 500 wild and cultivated hosts, including S. halepense (Khan 2007). Macrophomina phaseolina is widely present in soil and has been reported to cause yield losses of 30% to 50% in southern soybean production regions of the United States (McGee 1992; Yang and Navi 2005). In sorghum, up to 46.6% yield loss was recorded for susceptible plants with complete wilting and lodging (Arora and Dhurwe 2014). In a study in Australia, M. phaseolina has been isolated from the roots of symptomless plants of 23 weed species, including S. halepense (Fuhlbohm et al. 2012). In a recent study of genetic diversity of M. phaseolina in Senegal based on DNA sequences of five loci, internal transcribed spacer (ITS), translation elongation factor (TEF), actin (ACT), calmodulin (CAL), and tubulin (TUB), two clades were generated, but no consistent correlation was found among genotype, host, or geographic location, and isolates from both clades could even occur on the same host at the same location (Sarr et al. 2014). Another recent study suggested that five Macrophomina species can be defined based on DNA sequence diversity among isolates collected from oilseed crops in Brazil (Machado et al. 2019). However, no indications for host specificity were described. Thus, while S. halepense could serve as a source of inoculum on occasion, it seems unlikely that it has a large impact on the overall spread of the crop diseases caused by Macrophomina.

Curvularia spp. and Bipolaris spp.

Curvularia lunata (Wakker) Boedijn and Curvularia geniculata (Tracy & Earle) Boedijn have been isolated from typical leaf spot lesions of a wide range of hosts, including S. halepense (Pratt 2006). No clear indication of host specificity has been seen. In a test to examine host range, single spore cultures of C. lunata isolated from lesions of the pulse black gram [Vigna mungo (L.) Hepper] were grown and used to prepare high concentrations of inoculum (Lal et al. 2013). When sprayed onto 30-d-old plants of 58 plant species in seven families, other than for the only three Euphorbuaceae species tested, at least one species in the other six families developed leaf spot symptoms. While S. halepense was not tested, corn and rice (Oryza sativa L.) were positive, but Sorghum vulgare (a synonym of S. bicolor) was negative (Lal et al. 2013). In other cases, C. lunata has been shown to cause leaf spot disease on grain sorghum in Pakistan (Akram et al. 2014) and on sweet sorghum in China (Tong et al. 2016), both of which are S. bicolor. Curvularia lunata is also often identified as a cause of grain mold in sorghum (Bandyopadhyay et al. 1991; Prom et al. 2017b). In corn, C. lunata is reported to cause approximately 10% to 60% yield losses and up to 33.4% losses in grain yield under hot and humid conditions (Bisht et al. 2018; DingFa et al. 1999).

Curvularia geniculata also causes leaf spot on corn and has previously been isolated from S. halepense (Hodges and Madsen 1979). Moreover, C. lunata and C. geniculata are associated with leaf spots of Lacatan banana (Musa acuminata Colla) plants (Meredith 1963). In a recent study, C. geniculata was confirmed as the principal alfalfa (Medicago sativa L.) foliar pathogen in the Brazilian state of Rio Grande do Sul (Ávila et al. 2017). Based on a survey conducted of seed-borne fungal diseases of rice in Burkina Faso, incidence rate of C. geniculata was 0.5% to 2% (Ouedraogo et al. 2016).

Bipolaris halepense Chiang, Leonard & Van Dyke was isolated from diseased leaves of S. halepense in North Carolina in 1989 (Chiang et al. 1989a). Conidia of B. halepense resemble those of Bipolaris maydis (Y. Nisik. & C. Miyake) Shoemaker, a foliar pathogen of corn, but B. halepense is only weakly pathogenic to corn and did not mate with fertile isolates of either mating type of B. maydis (Chiang et al. 1989a). Symptoms from B. halepense when found on S. halepense lack the zonate pattern, so are more typical for the lesions caused by Bipolaris sorghicola (Lefebre & Scherwin) Alcorn (Manamgoda et al. 2014). B. sorghicola was found on S. halepense in La Plata, Argentina, and the diseased S. halepense plants were described as having leaf spots (Acciaresi and Mónaco 1999). Katewa et al. (2006) inoculated conidia of B. sorghicola to sorghum cultivars ‘IS164’ and ‘SU 45’, and the reduction in grain yields was near 50% in both cultivars compared with the control.

Bipolaris sorghicola is reported to cause target leaf spot on barley (Hordeum vulgare L.), onion (Allium cepa L.), Arabidopsis thaliana spp., and sorghum (Peng et al. 2016).

In a 2006 report by Pratt, besides C. lunata, and C. geniculata, Bipolaris cynodontis (Marig.) Shoemaker, Bipolaris spicifera (Banier) Subr, and Exserohilum rostratum (Drechs.) Leonard & Suggs (formerly Bipolaris halodes) were also recovered from symptomatic leaves of S. halepense. In this case, the S. halepense was growing in association with Bermudagrass [Cynodon dactylon (L.) Pers.]. Spores produced from cultures of the two Bipolaris species and E. rostatum were cross-infective to Bermudagrass, causing typical leaf spot symptoms (Brecht et al. 2007; Pratt 2006). Bipolaris cynodontis has also been isolated from rice (Zehhar et al. 2008). In Bangladesh, the major pathogen of leaf blight in wheat (Triticum aestivum L.) is Bipolaris sorokiniana (Sacc.) Shoemaker, but other fungal species such as Bipolaris cynodontis (Marig.) Shoemaker, Bipolaris oryzae (Breda De Haan) Shoemaker, Bipolaris tetramera (Mckinney) Shoemaker, and Bipolaris victoriae (Meehan & Murphy) Shoemaker have been also isolated from infected wheat leaves (Momtaz et al. 2019). Although it is not proven to cause severe disease, B. cynodontis was found in 10.4% of the rice seed lots from a total of 722 rice seed lots in Rio Grande do Sul, Brazil (Meneses et al. 2014). As in the case of Macrophomina, even if S. halepense is a host for these pathogens, based on their extensive host ranges, it seems unlikely that it regularly serves as a major source of inoculum for this group of pathogens.

It is important to note that C. lunata refers to the asexually reproducing form (anamorph) of an ascomycetous fungus that also has a sexually reproducing form (teleomorph) in the genus Cochliobolus. Because identification of Curvularia based primarily on conidial morphology is not highly discriminatory, efforts are being made to use DNA sequence information to sort out the phylogeny of the group. Index Fungorum ( http://www.indexfungorum.org/Names/Names.asp) lists 134 species of Bipolaris, 217 species of Curvularia, and 54 species of Cochliobolus, including C. lunatus, the presumed teleomorph of C. lunata. Several teleomorphs such as Cochliobolus heterostrophus (Drechsler) Drechsler are associated with serious diseases of specific hosts, including southern leaf blight of corn. When sequences of ribosomal ITS and a portion of the single-copy gene g3pd (glyceraldehyde-3-phosphate dehydrogenase, including 2 introns) for 41 species defined as Cochliobolus were subjected to phylogenetic analysis, the results grouped the isolates into two clusters (Berbee et al. 1999). For 16 species in cluster 2, the classification, if based on asexual spores, would be either Curvularia or Bipolaris. All species in cluster 1 (14 Cochliobolus species) were associated with Bipolaris as the anamorph. Addition of TEF and the large-subunit rRNA (LSU) sequences led to further reclassification of morphologically defined species of Curvularia and Bipolaris (Manamgoda 2015). In these studies, isolates from sorghum were classified into seven different species, none of which was C. lunata (Manamgoda 2015; Marin-Felix et al. 2020). Clearly, it will be important to use DNA sequence information to identify the species and to perform cross-species inoculation tests to determine whether Curvularia from S. halepense is a threat to neighboring crop species. The similarity of Curvularia and Bipolaris was not surprising, as each is known to derive from teleoforms of Cochliobolus. However, these observations show that isolates from different hosts described as separate species of Curvularia or Bipolaris in earlier literature may not meet today's species definitions. It is also possible that some are anamorphs derived from genetically distinct species that do have host specificity. (At one time these fungi were all classed as members of the genus Helminthosporium and later Drechslera.)

Exserohilum spp.

Exserohilum rostratum (or Setosphaeria rostatum when the name for the sexual stage is used), as stated previously, has been isolated from S. halepense and also appears to have a very wide host range. When E. rostratum isolates from banana were tested via assays using detached leaves from 128 different plant species belonging to 47 families, 60 developed leaf spot lesions. These included 17 of the 20 Gramineae tested, including corn (Lin et al. 2011). Exserohilum rostratum has been recovered from lesions on rice (Cardona and González 2007; Mahmad Toher et al. 2015), and it also causes leaf spot on bottle gourd [Lagenaria siceraria (Molina) Standl.] leaves (Choudhary et al. 2018) and pineapple (Ananas comosus (L.) Merr.] leaves (Luo et al. 2011). In July 2009, atypical symptoms of a leaf spot disease from which E. rostratum was cultured were observed on mature pineapple leaves in Chengmai County in China; approximately 15% of plants propagated from suckers became symptomatic after 150 to 300 d, eventually causing a 3% to 10% yield loss (Luo et al. 2011). Exserohilum rostratum has been implicated as causing root rot of lettuce (Lactuca sativa L.) (Alamri et al. 2019). Further, it is frequently mentioned as a pathogen in humans, as exemplified by Alajmi et al. (2019).

Based on results of greenhouse studies, a mixture of Drechslera gigantea (Heald & F.A. Wolf) S. Ito, Exserohilum longirostratum (Subram.) Sivan, and E. rostratum has been recommended as a biocontrol for S. halepense and six other weed species (Chandramohan and Charudattan 2001). The tests included inoculation of seedlings of six sorghum and six corn varieties as well as other garden and crop species that were all either resistant or immune. No follow-up reports on in-field applications were found.

Once again, the use of DNA sequence information, in this case from nine different regions, has led to significant reevaluation of Exserohilum spp. Most notably, E. rostratum was revealed as conspecific with other previously described Exserohilum species such as Exserohilum antillanum R.F. Castañeda, Guarro & Cano, Exserohilum gedarefense (El Shafie) Alcorn, Exserohilum leptochloae Y. Nisik. & C. Miyake, Exserohilum longirostratum (Subram.) Sivan., Exserohilum macginnisii A.A. Padhye & Ajello, and Exserohilum prolatum K.J. Leonard & Suggs. Isolates from sorghum still fell into seven different species, most commonly Exserohilum turcicum (Pass.) Leonard & Sugg. (Hernández-Restrepo et al. 2018).

Exserohilum turcicum is most widely known as the cause of northern corn leaf blight in corn (Chiang et al. 1989b). It is one of the most common and economically significant fungal leaf diseases of corn in the north-central United States and Ontario, Canada (Jindal et al. 2019; Weems and Bradley 2017), and this destructive pathogen can reduce the grain yield of corn by more than 90% (Pant et al. 2000). Other studies have shown mixed results as far as host specificity of isolates. Reports describing recovery from S. halepense include Chiang et al. (1989b), who found that S. halepense seedlings are susceptible to isolates recovered from Sorghum spp. (Sudan grass [Sorghum bicolor (L.) Moench ssp. drummondi (Nees ex Steud.) de Wet & Harlan], S. halepense, and broomcorn [Sorghum vulgare Pers. var. technicum (Koern.) Jáv.]); S. halepense has been identified as an overwintering host (Levy 1984). It can also provide a suitable medium in culture for crosses involving the teleomorph (Setosphaeria turcica) (Moghaddam and Pataky 1994). Sorghum host differentials have been identified in India that show varying responses across locations, indicating that multiple pathotypes are present (Mathur et al. 2011). However, lack of cross infection between corn and S. halepense isolates has also been reported (Abadi et al. 1996). In one study, an E. turcicum originally isolated from S. halepense in Italy was inoculated to 40 varieties of cultivated sorghum, 25 hybrids of corn, and 5 varieties of durum wheat, bread wheat, oat (Avena sativa L.), barley and rice. Overall, only 15 varieties of cultivated sorghum showed a mild level of infection (Del Serrone and Fornasari 1995). In a similar study, a North Carolina isolate of E. turcicum that had been isolated from S. halepense caused moderate to severe damage to sorghum and corn (Chiang et al. 1989c). So, S. halepense may well act as a significant reservoir for E. turcicum.

Claviceps Africana

Sorghum ergot, caused by Claviceps africana Frederickson, Mantle & De Milliano, is a disease that replaces the seed on panicles of infected florets with sphacelia/sclerotia (Odvody et al. 2002). In India, losses of 10% to 80% have been reported in hybrid seed production fields, and ergot epiphytotics in Zimbabwe result in regular annual losses of 12% to 25% and occasionally in total losses (Bandyopadhyay et al. 1998). Although now global in nature, sorghum ergot was not known to be in the Western Hemisphere before 1995. After being reported in Mexico (Velasquez-Valle et al. 1998), it was later seen in Texas in the lower Rio Grande valley, where it was found in both sorghum fields and adjacent stands of S. halepense (Isakeit et al. 2007). Because of the mild climate in the Rio Grande region, conidia can be produced year-round, providing a continual source of inoculum. Consequently, S. halepense has been suggested as a likely source of recurring disease (Odvody and Isaskeit 1997; Prom et al. 2005), allowing annual spread throughout U.S. sorghum production regions as the growing season advances northward.

Sporisorium cruentum

In a greenhouse study, teliospores of Sphacelotheca holci Jack. [= Sphaceloiheca cruenta (Kühn.) Potter] (synonym to Sporisorium cruentum (Kühn) K. Vánky), that causes loose kernel smut in sorghum, infected S. halepense systemically after inoculation of cut stems (Massion and Lindow 1986). S. cruentum has been suggested as a biological control for S. halepense (Millhollon 2000), but isolates from S. halepense also cause loose kernel smut in sorghum as reported by Dean (1966). Recently, a sample from S. halepense was shown to readily infect sorghum cultivar ‘BTx643’ plants (Prom et al. 2017a), making any use to control S. halepense a potential problem for nearby sorghum. In Ethiopia, the incidence of covered kernel smut is estimated to be around 50% (Azanaw et al. 2020; Mengistu 1982).

Colletotrichum sublineola

Before 1992 (and sometimes since) the species name graminicola was used to identify pathogens in the genus Colletotrichum that cause anthracnose on corn, sorghum, and other gramineae crops, with some isolates being identified as having restricted host specificity. However, based on differences between perfect stages (Glomerella) (Vaillancourt and Hanau 1992) and ITS sequencing (Sherriff et al. 1995), Colletotrichum sublineola Henn. ex Sacc. & Trotter 1913 (or sublineolum) is now used for isolates that infect sorghum. Sorghum halepense isolates of C. sublineola, have been shown to infect sorghum cultivars (Xavier et al. 2018). Conversely, under ideal conditions in a greenhouse, only inoculation at late growth stages of S. halepense led to infection by C. sublineola isolates originating from grain sorghum (Ahn et al. 2020). In 1989, it was reported that C. graminicola extracted from S. halepense caused moderate to severe leaf damage on corn and sorghum; even oats and barley were slightly affected by this isolate (Chiang et al. 1989c). However, this was before the separation of the species names graminicola and sublineola in 1992, so the identity of the Colletotrichum isolate used in the study is not clear, nor is it known whether other species also can reproduce on S. halepense. In sorghum, losses caused by the panicle phase of anthracnose in terms of grain yield are generally 2% to 15% but may be up to 30% to 50% (Frederiksen and Odvody 2000), so S. halepense and possible other alternate hosts do pose a potential threat for sorghum production.

Gloeocercospora sorghi

Gloeocercospora sorghi Bain & Edgerton causes zonate leaf spot on sorghum and has been recovered from S. halepense showing the same symptoms (Chiang et al. 1989a). Inoculation with an isolate of G. sorghi from S. halepense caused damage to corn and sorghum; mycelial growth and sclerotia appeared on incubated leaves of Sorghum spp. but not other species, which indicates that G. sorghi was compatible only with Sorghum spp. (Chiang et al. 1989c). Although the distinctive pattern of infection of sorghum leaves show it is a very common disease, it seems not to cause sufficient levels of yield loss to stimulate further research. Gloeocercospora sorghi has been tested as bioherbicide for S. halepense (Mitchell et al. 2003), but the paper also pointed out it was highly virulent in other sorghums.

Ramulispora sorghicola

Oval leaf spot caused by Ramulispora sorghicola E. Harris was observed on sorghum and S. halepense near Beeville, TX, during August 2002 (Odvody et al. 2006). The observation that rows of sorghum nearest to S. halepense displayed the same symptoms and that conidial cultures were found to reproduce the disease on both hosts implies that S. halepense was serving as a spreader. In winter months, oval leaf spot was mostly found on S. halepense, further strengthening the idea that S. halepense was the primary source. Because resistant sorghum cultivars are available, R. sorghicola has not led to significant sorghum yield losses (Odvody et al. 2006).

Rhizoctonia solani

Rhizoctonia solani Kühn [teleomorph Thanatephorus cucumeris (A.B. Frank) Donk.], an undefined binucleate Rhizoctonia, and Rhizoctonia zeae Voorhees (teleomorph Waitea circinata Warcup & Talbot AG Z) were isolated from S. halepense growing in Turkey (Demirci and Eken 1999; Demirci et al. 2002). Rhizoctonia solani is a soilborne plant pathogen with considerable diversity in cultural morphology, host range, and aggressiveness (Ajayi-Oyetunde and Bradley 2018). Heterokaryon compatibility subdivides the species into 14 anastomosis groups that may differ in host range, several of which (AG-1A AG1B, AG4, and AG-5) have been isolated from corn (Li et al. 1998) and, except for AG-1B, from sorghum (Gao 1987). AG-1 isolates are also pathogens of soybean, and soybean isolates have been shown to infect S. halepense (Black et al. 1996). The R. solani that causes severe seedling damping-off up to 80% to 100% and final yield loss of up to 30% of oilseed rape (Brassica napus L.) worldwide belongs to AG2-1 (Kataria and Verma 1992; Khangura et al. 1999; Sturrock et al. 2015; Tahvonen et al. 1984).

While R. zeae derives its name from a corn disease described in 1934 (Voorhees 1934), it has also been reported to infect turfgrass in Florida, Ohio, and Ontario (Elliott 1999; Hsiang and Masilamany 2007) and rice (Sifat and Monjil 2017). More research is required to determine whether S. halepense serves as a source of Rhizoctonia diseases of crop species and, if so, which of the anastomosis groups are involved.

Sporisorium reilianum

Sporisorium reilianum (J.G. Kühn) Langdon & Full. (formerly Sphacelothca reiliana), the cause of head smut in sorghum and corn, may represent an exception where S. halepense is not a host. Yield losses attributed to S. reilianum are estimated to be as high as 80% in corn (Frederiksen 1977; Jin et al. 2000; Yu et al. 2014). Attempts to create infections using sporidia from cultures derived from teliospores collected from infected sorghum did not produce infection from spray, needle, or root-dip inoculation on any of several S. halepense cultivars tested (personal observations).

Xanthomonas vasicola

Xanthomonas vasicola pv. Vasculorum causes bacterial leaf streak in corn, and in a recent study, it was revealed that S. halepense is an alternative host of X. vasicola (Hartman 2018). That study also showed that cultivars of grain sorghum, oats, and rice also developed symptoms when inoculated with bacterial cultures grown from a corn isolate. The same bacterium is known to cause gummy disease of sugarcane (Hartman 2018). The impact of bacterial leaf streak on yield is not yet known, but it is not considered a major disease on crops (Byamukama et al. 2020).

Xylella fastidiosa

Xylella fastidiosa, a common bacterial pathogen that causes Pierce's disease in grapes (Vitis aestivalis Michx.), was found in S. halepense in 1959 (Turner and Pollard 1959). More recently, inoculation of weed species with sharpshooter insects [Homalodisca vitripennis (Germar), formerly known as H. coagulate (Say); Xyphon fulgidum (Nottingham); and Graphocephala atropunctata (Signoret)] previously fed on infected grapes for 4 d found that 14 of 62 inoculated S. halepense plants maintained detectable levels of the pathogen, with systemic spread in two of the plants (Wistrom and Purcell 2005). However, an assay made the following year showed that many other weeds in almond [Prunus dulcis (Mill.) D.A. Webb] orchards in the same region also harbored X. fastidiosa, and in that survey, no positive tests were found on S. halepense (Shapland et al. 2006).

The cost of Pierce's disease in California is approximately $104.4 million yr^–1 (Tumber et al. 2014), so weed as well as insect control measures are warranted.