Spot blotch (SB) caused by the hemibiotrophic fungus Bipolaris sorokiniana (teleomorph Cochliobolus sativus) syn. Drechslera sorokiniana, syn. Helminthosporium sativum is the most devastating disease of wheat grown in warm and humid areas. In Eastern Gangetic Plains (EGP) of India, Bangladesh and Nepal, B. sorokiniana appears in a complex with Pyrenophora tritici-repentis (Died.) Drechs. (anamorph Drechslera tritici-repentis (Died.) Shoemaker) responsible for tan spot (TS) and is commonly known as Helminthosporium leaf blight (HLB) (Duveiller et al., 2005). Occurrence of SB is more frequent in the humid and warmer wheat growing areas of South Asia (SA), Latin America and Africa (He et al., 2022) ( Figure 1 ). Globally, the disease appears in approximately 25-million-hectare (mha) areas, out of which 10 mha areas are present in EGP. Besides, wheat grown under subtropical lowland of Bolivia, Brazil and Argentina in Latin America, Tanzania, rainfed areas of Zambia and Madagascar in Africa provides congenial environments for SB (van Ginkel and Rajaram, 1998). Under favorable conditions, the disease may cause yield loss of above 50% (Sharma and Duveiller, 2004), with an average yield loss of 15-20% in SA, and yield loss in the farmer’s field reported up to 16% in Nepal and 15% in Bangladesh (Villareal et al., 1995; Saari, 1998; Duveiller, 2002).

B. sorokiniana causes a typical symptom of light brown colored lesions of oval or oblong to elliptical shape on leaves, sheath, nodes or glume of its host plants. Size of the lesion gradually increases, then partial to whole leaf may become chlorotic, turning brown and drying up ( Figure 2 ). The pathogen transmits through infected seeds, stubbles and soil, and secondary infection may take place through air. Other than SB, B. sorokiniana is also responsible for seedling blight, common root rot, head blight and black point in wheat (Al-Sadi, 2021). No positive association was found among spot blotch, root rot and black point in wheat, indicating that different mechanisms of host resistance exist in different plant parts (Conner, 1990). Cross infection between different species is rarely reported; one such example is isolates collected from wheat root were able to infect barley (Valjavec-Gratian and Steffenson, 1997). A number of articles have been published pertaining to pathogen biology, disease management, breeding and molecular aspects, including genome sequence of B. sorokiniana, gene/QTL mapping, marker-assisted selection (MAS) and genomic selection. The present work aims to summarize the most important findings, especially those reported in recent years, in the area of SB management in wheat.

The pathogen produces olive brown mycelia and light grayish colonies on potato dextrose agar (PDA) medium at early stage, which turns into black at later stage. Conidia are brown colored, elliptical, straight or curved multiple celled with 3-9 septa tapering at the ends, measuring 10-28 × 40-120 µm (Acharya et al., 2011). Variability under natural conditions among the B. sorokiniana isolates is sufficiently high (Sultana et al., 2018). Bipolaris sorokiniana is the asexual stage of the pathogen, which multiplies mostly through conidia. Its sexual stage has not been reported in natural conditions except in Zambia, due to a lack of sexual compatibility between the opposite mating (A, a) types. Under controlled conditions, sexual spores of B. sorokiniana were isolated from barley (Zhong and Steffenson, 2001) and recently from wheat in Bangladesh (Sultana et al., 2018).

The fungus can produce toxins like helminthosporol and hydrolytic enzymes that trigger pathogenesis. Prehelminthosporium is the most abundant and active compound produced by B. sorokiniana, which damages membrane permeability and affects mitochondrial oxidative phosphorylation and chloroplast photophosphorylation (Kumar et al., 2002). A necrotrophic effector gene ToxA interacts with the susceptibility gene Tsn1 in wheat to initiate disease development (McDonald et al., 2017). ToxA was initially identified in P. tritici-repentis and then in Parastagonospora nodorum, but molecular evidence indicated that the gene in the former was acquired from the latter through horizontal gene transfer (Friesen et al., 2006). ToxA was found in B. sorokiniana populations from Australia (McDonald et al., 2017), USA (Friesen et al., 2018), India (Navathe et al., 2019b) and Mexico (Wu et al., 2020), with various occurrence frequencies, from 10.2% in Mexico to 86.7% in USA.

Molecular markers may be useful to detect the pathogen on wheat plants before the appearance of visible symptoms, as well as on alternative hosts and volunteer plants. A sequence characterized amplified region (SCAR) marker SCARBS₆₀₀ was developed to diagnose B. sorokiniana (Aggarwal et al., 2011). Alternatively, DNA sequence of ribosomal internal transcribe spacer (ITS), β-tubulin gene and translational elongation factor 1-α (EF-1α) can also be used to diagnose this pathogen, as did in a study to detect B. sorokiniana in volunteer plants in China (Sun et al., 2015). Using universal rice primers (URP), Aggarwal et al. (2010) successfully grouped 40 B. sorokiniana isolates from different geographical origins of India. High level of genetic diversity among the isolates from Brazil and Mexico was reported using UPR markers (Mann et al., 2014).

Draft genome sequences of eight virulent accessions of B. sorokiniana from India, Australia, USA and China are currently available (https://www.ncbi.nlm.nih.gov/data-hub/genome/?taxon=45130). A highly virulent isolate BS_112 (GenBank accession number KU201275) from India has a genome size of 35.64 Mb and 10,460 genes were predicted with an average gene length of 435-545 bp and gene density of 250-300 genes/Mb (Aggarwal et al., 2019). A phylogenetic analysis was carried out among 254 isolates of B. sorokiniana with global origin using gene sequences of ITS, TEF-1 and GAPDH, and the results indicated the presence of a broad and geographically undifferentiated global population (Sharma et al., 2022).

Bipolaris sorokiniana initially has a biotrophic phase represented by the epidermal invasion and fungal hyphal growth, followed by the necrotrophic phase in the mesophyll cells (Kumar et al., 2002). The germinating conidia penetrates the cuticle and epidermis of wheat plant with the help of an appressorium at its germinating tube, getting entered mostly through the anticlinal cell walls. The levels of sesquiterpene molecule ‘prehelminthosporol’ increases in the extracellular matrix of the cell at the site of apposition, helping pathogen to intrude further into the cell (Jansson and Akesson, 2003).

The first toxin compound known to confer virulence to B. sorokiniana was named ‘Victoxinin’ and the second one was ‘sorokinianin’. Another toxin isolated and characterized was ‘bipolaroxin’, which was again structurally a sesquiterpene and had a role in pathogenicity and host selectivity (Jahani, 2005). Helminthosporol was found to enhance the susceptibility of genotypes like Sonalika and CIANO T79. However, it is important to note that helminthosporol and its derivatives are not solely responsible for deciding the susceptibility of a genotype. A multitude of other factors like cell wall apposition, cuticle thickness, leaf anatomy, pathogen specificity, host defense responses etc., are also involved in the pathosystem, making both resistance/susceptibility of the host and virulence/avirulence of the pathogen (Ibeagha et al., 2005; Jahani et al., 2014).

For initial invasion, B. sorokiniana produces various cell wall degrading enzymes like glucosidase, cellulases, pectinases, xylanase. Endopolygalacturonase (EPG) loosens the cell wall by cleaving α-(1→4) linkages of the homogalacturonan, an important constituent of the middle lamella of the cell wall (Ridley et al., 2001; Janni et al., 2008). To protect the host cell from EPG, plant cell produces polygalacturonase inhibiting protein (PGIP), which elicits the defense response of a plant by accumulating oligogalacturonides (Ridley et al., 2001). PGIPs have a proven role against the fungal colonization in many dicot species as well as wheat plant against Bipolaris (Kemp et al., 2003).

Generally, temperature between 16-32°C enables SB development (Acharya et al., 2011), and in Indian subcontinent, the disease predominantly spread when temperature exceeds 26°C as it favors heavy sporulation (Chaurasia et al., 2000). Teleomorph develops in a range of 16-24°C with the optimum temperature of 20°C and can survive up to seven months under natural conditions in Zambia; while the anamorph can survive sufficiently large range of temperature from 4-36°C (Duveiller and Sharma, 2009). High temperature and high relative humidity enhance disease severity, SB outbreak in Brazil occurred when the leaves remain wet for >18 hrs in a day with a mean temperature of >18°C (Reis, 1991). In EGP, leaf wetness period >12hrs due to rainfall or dew coinciding with high temperature and humidity are believed to favor the onset of infection (Duveiller et al., 2005). In addition, delayed sowing of wheat due to the rice-wheat cropping system causes yield loss due to terminal heat stress (Hasan et al., 2021; Narendra et al., 2021); besides, high residual soil moisture and increased duration of leaf wetness due to foggy weather can also increase the disease severity (Duveiller, 2004; Duveiller et al., 2005). The waterlogged condition due to flooding in the Ganges belt sharply declines the conidia viability, and B. sorokiniana conidia isolated from soil after August, the monsoon month with high rainfall, becomes non-pathogenic (Pandey et al., 2005). This in turn implies that seeds might be the main source of inoculum in EGP.

SB is a polycyclic disease with the initial sources of inoculum being contaminated seeds, infected soil, straw, volunteer plants and secondary hosts. B. sorokiniana has a large host range, and more than 65 graminaceous hosts have been identified in China (Chang and Wu, 1998). Among the cereals, hexaploid wheat and barley are most common hosts, along with durum and emmer wheat, triticale, oats, rice, rye, maize, pearl millet, foxtail millet and several grass species like Phalaris minor, Agropyron pectinatum, A. repens, Festuca spp. (Gupta et al., 2017). A list of plant species that harbors B. sorokiniana is given in Table 1 . The three most common species, Setaria glauca, Echinochloa colonum and Pennisetum typhoids act as a natural harbor of B. sorokiniana in EGP (Pandey et al., 2005). In rice-wheat cropping system, rice plants may serve as a host for the pathogen (Acharya et al., 2011); but in eastern India the source of primary inoculum is still debatable, with infected seeds and weeds being the most probable inoculum sources (Neupane et al., 2010).

Management of SB through resistant varieties is the most economical and environment-friendly approach, which, however, is compromised by a lack of highly resistant varieties. Under this circumstance, cultivation of resistant varieties may be supplemented with other strategies like adjusting sowing time and fungicides application to reduce the SB severity in disease prone areas. Details of these strategies are described below.

Quantitative nature of SB resistance is predominantly reported in wheat (Singh et al., 2018; Bainsla et al., 2020; He et al., 2020), but reports are also available for major gene(s) governing SB resistance. Single dominant gene was postulated in the resistant genotypes Chirya 3 and MS#7 when they were crossed with common susceptible parent BL1473 (Neupane et al., 2007). Likewise, single dominant gene was reported in the resistant genotype DT 188, whereas digenic dominant resistance was reported in the lines E5895, HD 1927 and Motia (Adlakha et al., 1984). More genes were estimated in other resistant varieties, e.g., 2-3 genes in Gisuz, Cugap, Chirya 1 and Sabuf (Velazquez-Cruz, 1994), and three genes in Acc.8226, Mon/Ald and Suzhoe#8 (Joshi et al., 2004b). Populations in these two studies have already began to show a pattern similar to polygenic segregation, implying that most resistant sources are governed by multiple genes with minor effects, which increases the chances of deriving transgressive segregants in the progenies (Singh et al., 2018; He et al., 2020). The magnitude of heritability (h² ) for SB resistance varied greatly in different studies, e.g., from 0.21 to 0.64 in Sharma et al. (2006b) and 0.85 to 0.89 in He et al. (2020), whereas most studies exhibited moderate to high heritability, providing a good opportunity to select resistant genotypes in breeding programs.

Gene silencing through RNAi is a powerful tool for controlling insects, nematodes, viruses, fungal diseases like powdery mildew, and rusts (Qi et al., 2019). Utilization of RNAi in functional genomic analysis in B. sorokiniana was reported by Leng et al. (2011), and it can be further explored in SB pathogenesis and resistance breeding in wheat.

Liu et al. (2012) developed a new mapping strategy combining bulk segregant analysis and RNA-Seq called ‘BSR-Seq’, where transcripts are sequenced from extreme bulks, being a potential technique for marker discovery in large polyploid genome like wheat. Using BSR-Seq, five SB-resistance associated transcripts were identified on 5B and 3B chromosomes and their potential role in SB resistance were inferred (Saxesena et al., 2022).

Transgenic lines expressing foreign genes proved to be a potential approach to control insect and diseases in several crop plants. Examples include the heteroexpression of PvPGIP2 (Janni et al., 2008) and overexpression of TaPIMP1 and TaPIMP2 (Zhang et al., 2012; Wei et al., 2017) in transgenic wheat lines that enhanced the resistance against B. sorokiniana. However, government regulations on transgenic development are major concerns for researchers.

Additional techniques like genome editing (Zhang et al., 2017) and Eco-Tilling (Ajaz et al., 2021) have been increasingly utilized in wheat, having great potential to contribute to SB resistance breeding in near future.

Spot blotch is a disease of concern in warmer wheat growing areas of South Asia, Latin America and Africa. Most of the commercially grown cultivars are moderately resistant to susceptible and are subjected to significant yield losses under conducive climatic conditions. An integrated disease management strategy involving cultural practices, chemical control, resistant cultivars, etc., is needed to combat the disease. In addition, modern biotechnology brings new tools for the rapid and efficient development of resistant cultivars in wheat.

CR, XH, and PS conceptualized the manuscript. CR drafted the first version. NG and SM collected information and improved the first draft. XH and PS edited and approved the submitted version. All authors contributed to the article and approved the submitted version.