Unraveling the mystery of dieback in Dalbergia sissoo: a review

Abstract

The shisham tree (Dalbergia sissoo) is a keystone hardwood species of South Asia, highly valued in economic value in forestry, agroforestry, and landscape horticulture due to its durable, fragrant, and decay-resistant wood. However, shisham's health on both public and private lands is seriously compromised by recurrent outbreaks of dieback disease. Shisham has a history of severe dieback over the last century throughout its natural and introduced range. Since 1918, mortality associated with shisham dieback has been studied to determine its spread and underlying causes. Like most pathosystems, shisham dieback involves complex interactions among multiple biotic and abiotic factors, with certain site- and stand-level factors exacerbating disease severity across various regions and times. Recent outbreaks of shisham dieback in Pakistan have been linked to Ceratocystis dalbergicans. Previously, Fusarium was linked to wilt/dieback disease in Shisham. This disease has been differentiated from often-confusing Fusarium wilt/dieback on the same plant and explains dieback, a separate disease of shisham. Currently, published guidelines for managing Ceratocystis infections in shisham are limited. While researchers have explored potential management strategies, including identifying host resistance genes and chemical control methods, achieving sustainable disease control will require long-term, dedicated efforts due to the extended lifespan of shisham trees. This review provides a historical and updated perspective on the investigation and establishment of the pathogenic basis of shisham dieback, focusing on the role of Ceratocystis species. This work aims to clarify existing knowledge gaps, resolve controversies surrounding disease causation, and inform future research to enhance shisham conservation efforts.

Background

Shisham (Dalbergia sissoo) is a moisture-loving, fast-growing, medium- to large-sized deciduous tree in the family Fabaceae (CABI 2021a), native to the Indian subcontinent (Javed et al. 2023b). This species is economically important due to its durable and decay-resistant wood, valued for construction, furniture, and marine-grade plywood (Tewari 1994). Beyond economic uses, shisham has medicinal and industrial utility: it is a source of fuel, alkaloids, fibers, neoflavanoids, resins, and tannins (Kumar and Khurana 2016; Ijaz and Ul Haq 2021). It is used in large-scale timber production and cultivated as a landscaping tree in urban areas, parks, schools, and highways, where it acts as a vital sink for airborne pollutants (Ghosh 2018; Latif et al. 2023). In South Asian traditional medicine, the wood and bark have been recognized for their abortifacient, antipyretic, anthelmintic, aphrodisiac, and expectorant properties (Shah et al. 2010; Kumar and Khurana 2016), while the seed oil and powdered wood are used for treating skin ailments (Shah et al. 2010). Its leaves are used as animal feed and provide habitat for wildlife species such as vultures, which are critically endangered in Pakistan (WWF 2021). Shisham trees form symbiotic relationships with nitrogen-fixing rhizobacteria on their roots, improving nutrient availability in the soil (Kumar and Khurana 2016).

The terms ‘decline’, ‘dieback’, and ‘wilt’ classify three distinct diseases based on symptoms. The term ‘decline’ often describes a more general set of symptoms associated with loss of tree vigor (for example, foliage death, reduced growth, or premature foliage dropping). The term ‘dieback’ can be defined as the ‘progressive death of shoots, branches, and roots, generally starting at the tip, and associated with changes in soil moisture or virulent pathogens’. A decline is an episodic event characterized by premature, progressive loss of trees and stand health over a given period without obvious evidence of a single causal factor, such as physical disturbance or attack by an aggressive disease or insect. Despite having a distinct meaning from ‘dieback’, ‘decline’ and ‘dieback’ have been used interchangeably to describe tree conditions. Symptoms of dieback and decline are also often mistaken for ‘wilts’, which are more specifically a ‘loss of rigidity and drooping of plant parts, generally caused by insufficient water in the plant’ (Ciesla and Donaubauer 1994; Agrios 2005; Fraedrich 2020; Asiegbu 2022).

Shisham dieback is a growing concern in the Indo-Pak subcontinent, posing a threat to this valuable species (Naqvi et al. 2019; Ul Haq et al. 2023). Research on shisham dieback has historically focused on the immense economic importance of the host (Ijaz and Haq 2021; Javed et al. 2023a). While many pathological studies have been conducted on shisham dieback disease, they often have conflicting results. In recent years, increasing mortality due to dieback has created a need among researchers to gather information about the rate of the disease and its causes. Shisham dieback due to Ceratocystis infection received significant attention a decade ago.

With a focus on the emerging pathogen Ceratocystis, associated with shisham mortality, we gathered in-depth knowledge over the century, the related questions and controversies, and summarized the current scientific understanding of shisham dieback disease. The novelty of this document is that it describes multiple potential drivers (biotic and abiotic) that have been reported since the early 1900s and can be attributed to this disease. This review provides new insights into the pathology of shisham dieback. This study aimed to determine how pathologists perceive shisham dieback.

Shisham dieback disease

Dieback is the most important and commonly found disease on shisham across much of the Asian subcontinent. Research has primarily aimed to trace the onset and proliferation of the disease, as well as to identify its causative agents (Naqvi et al. 2019; Ijaz and Ul Haq 2021). Since the early 1900s, successive outbreaks of shisham dieback have been observed in Bangladesh, India, Nepal, and Pakistan (Dayaram et al. 2003; Sah et al. 2003; Webb and Hossain 2005; Shakya and Lakhey 2007; Vogel et al. 2011; Mukhtar et al. 2014b). In the past 100 years, widespread dieback outbreaks and infestations have drastically reduced shisham densities and killed billions of shisham trees (Naqvi et al. 2019; Ul Haq et al. 2023). Although dieback has been present for more than 100 years and many scientific studies have been conducted, the widespread loss of shisham trees is still a problem today. The disease spreads rapidly and is present in most shisham-growing countries, causing a dramatic decline in shisham populations. The increasing prevalence of this disease indicates that it will cause significant economic losses in the future and may result in the extinction of this valuable tree species.

Shisham dieback disease symptoms

Affected shisham trees exhibit a range of symptoms, including yellowing, necrosis, thinning of leaves and crown, branch dieback at the initial and lateral stages, branch mortality, canopy loss, gummosis, vascular discoloration, and eventually tree death (Khan et al. 2000; Mukhtar et al. 2014b). Dieback-affected trees often exhibit bark cracking due to pressure pads and fungal mats growing just under the bark (Poussio et al. 2010; Latif et al. 2021). Fungal growth can block the flow of water and nutrients, causing the discoloration and wilting of leaves from the tops of trees and downward (Al Adawi et al. 2009, 2013; Latif et al. 2021; Javed et al. 2023a). Affected leaves may remain attached to the tree for some time or fall, and the crown progressively thins until the entire tree dies (Latif et al. 2021). Diseased trees show significant moisture reduction in and above the infected portion of the stem (Latif et al. 2021, 2023). Shisham trees die slowly at some locations, one to a few branches at a time, a process that can take from a few months to a few years. At other locations, there have been anecdotal reports of rapid wilting and death of the whole tree. Longitudinal bluish to grayish streaks just beneath the bark can extend several meters up the tree's stem and are a diagnostic symptom associated with shisham dieback (Figs.1, 2; Latif et al. 2021). These symptoms distinguish dieback from Fusarium wilt, which typically produces pink staining in xylem vessels (Haq et al. 2023; Latif et al. 2023; Bakshi and Singh 1954).

Fig. 1

Disease symptoms of shisham plants infected with Ceratocystis sp., and variability in disease symptoms. a Healthy shisham tree growing in natural conditions. b dieback infected tree showing thinning of leaves and crown. c shisham tree with partial dieback symptoms. d stag-headed dead tree. e excessive gummosis on tree stem. f bark splitting. g wilting throughout the crown of the tree, resembling physiological wilt or drought stress. h epicormic shoots of dieback infected tree, but eventually succumb to the infection. i one-sided wilting. j vascular discoloration (blue streaking along xylem vessels) just beneath the bark. k vascular blockage of xylem vessels (Latif et al. 2023)

Fig. 2

Shisham dieback diagnostic signs and symptoms. a diseased shisham tree showing vertical bark cracking due to pressure pads/mycelial mat formation. b fungal mats of Ceratocystis dalbergicans on a recently killed shisham tree, serving as a diagnostic symptom of shisham dieback disease. c another diagnostic feature is vascular streaking. Photo credit: Muhammad Zunair Latif

Century-locked secrets of dieback in shisham

The earliest records of shisham mortality date back to Nepal in the early 1900s. Since then, shisham mortality has become a significant concern in many areas where this tree is cultivated. The first systematic research on the etiology of dying shisham was initiated in 1915 by Parker, who claimed that Fomes lucidum was the cause of widespread tree death (Parker 1918). This initiated widespread and significant scientific debate over dieback outbreaks and their possible causes. Although many biotic and abiotic factors may contribute to the severity of outbreaks, researchers generally agree that fungal plant pathogens are primarily responsible for dieback symptoms. Parker's work was supported by the findings of two other scientists who published similar results (Troup 1921; Sharma et al. 2000). Many researchers have identified Fusarium solani as the leading cause of shisham mortality. Bagchee (1944) reported that F. solani was involved in wilt and dieback diseases of shisham. (Bakshi and Singh 1954) studied the host-parasite relationship and behavior of associated fungi both in vitro and in planta. He also studied the cause of pink stains in dieback-affected trees. (Bakshi 1955) investigated shisham mortality in natural and artificial plantations. He claimed that F. solani is comparatively more virulent under drought conditions. The fungus mainly attacks tree roots and blocks vascular bundles, ultimately leading to tree death. Bakshi (1957) reported on the correlation between edaphic factors and disease caused by Fusarium spp. (Bakshi and Singh 1959) concluded that F. solani is restricted to roots and that symptoms caused by this pathogenic fungus could be reproduced by artificial inoculation. Bakshi (1976) explained the role of Fusarium spp. in shisham root infections.

In 1998, a massive dieback outbreak occurred on the irrigated plains of Punjab, Pakistan, and losses of up to 70% were observed (Naz 2002). Gill et al. (2001) reported that shisham trees grown on canal sides and at other moist locations were susceptible to dieback disease caused by Phytophthora cinnamomi. Sah et al. (2003) explained the role of edaphic factors in shisham decline in Nepal. Various physical soil characteristics were analyzed, including pH, water-holding capacity, soil texture, soil density, soil porosity, and soil color. No correlation between the physical soil factors and shisham decline was found. (Dayaram et al. 2003) outlined the losses caused by F. solani f. sp. dalbergiae. Khan et al. (2004) investigated different fungi (B. theobromae, F. solani, and Colletotrichum sp.) associated with tree parts, but only B. theobromae was shown to be pathogenic in artificial inoculation experiments. Shakya and Lakhey (2007) confirmed that F. solani is the leading cause of dieback in Nepal. Javaid (2008) noted the maximum mortality of shisham plantations along bank canals and less mortality in agricultural fields. Younger trees were reportedly more resistant than older trees. Additionally, drought and high soil moisture content favor pathogen growth and disease severity. Rajput et al. (2008) reported that F. solani was the leading cause of dieback disease in shisham in Sindh, Pakistan.

Vogel et al. (2011) identified unknown viruses from dieback-affected trees in Bangladesh that might play an unknown role in disease. Rehman et al. (2012) reported that disease incidence is greater in irrigated plantations (53%) and lower in farmlands (8.3%). They identified F. solani as the most frequent fungus, followed by B. theobromae and P. cinnamomi, which were associated with roots, twigs, and bark samples. Ahmad et al. (2013) and Arif et al. (2013) suggested that Fusarium spp. is among the most significant genera of fungi contributing to disease. In Bangladesh, Valdez et al. (2013) described the potential role of three different strains of Pseudomonas in dieback disease. Mukhtar et al. (2014a) conducted comprehensive research in different ecological zones of Pakistan's Punjab and Sindh provinces and reported that dieback was prevalent at all study sites with varying degrees of severity. They also noted that disease incidence was greater in the rain-fed and northern irrigated plains of Punjab and was lower in sandy deserts. They concluded that environmental factors (temperature and moisture) play a crucial role in disease development and spread. Their findings confirm previous work showing that the F. solani complex can cause dieback in Punjab, Pakistan. According to Kumar and Khurana (2016), F. oxysporum and F. solani are pathogenic to shisham both together and alone. Poussio et al. (2010) reported that decreased shisham populations in Pakistan were due to Ceratocystis fimbriata. Al Adawi et al. (2009) consistently isolated Ceratocystis sp. from partially to wholly wilted shisham trees in Pakistan. Haq et al. (2019) summarized the associations of different isolates of C. fimbriata with shisham trees commonly affected by dieback disease from different districts of Pakistan. According to the latest research performed in Pakistan, shisham dieback disease prevails in different shisham-growing areas of Pakistan, and tree dieback severity varies among these dieback hotspots. Research has also concluded that environmental variables (rainfall, temperature, and relative humidity) influence disease development (Latif et al. 2021). Research indicated that 23 Ceratocystis sp. (Fig. 3) and 4 Fusarium sp. (Fig. 4) were isolated from infected tissues of shisham trees, and their potential to cause disease was examined in three shisham age groups. They found no evidence that dieback is caused by Fusarium sp., thus establishing that Ceratocystis sp. isolates are the root cause of the disease (Latif et al. 2023; Haq et al. 2023). The operational taxonomy of Ceratocystis isolates was explored using seven genetic loci, ITS, TEF1-α, RPBII, CAL, MS204, MCM7, and β-tubulin, and it was discovered that these isolates represent a new species, Ceratocystis dalbergicans, in the C. fimbriata sanu latu complex (Haq et al. 2023). However, Javed et al. (2023a) and Javed et al. (2023b) associated shisham dieback with prolonged exposure to drought, water logging, and salinity in nonnative planting sites of shisham trees in Pakistan, whereas insects and fungi were the secondary pathogens.

Fig. 3

Morphological features of Ceratocystis dalbergicans isolated from diseased shisham trees in Pakistan. a, b ascomata on wood chip of diseased shisham tree with masses of ascospores. c, d pure colonies of on PDA. e septate, hyaline to dark brown mycelia and cylindrical conidia. f aleuriconidia. g ascomata with masses of ascospores emerging from their necks. h barrel shaped conidia. i chlamydospores. All the pictures by Muhammad Zunair Latif, except c, d by Latif et al. 2023

Fig. 4

Morphological features of Fusarium sp. isolated from shisham trees in Pakistan a, b pure colonies on PDA. c, d micro- and macroconidia. All the pictures by Muhammad Zunair Latif, except c, d by Latif et al. 2023

Taxonomy of Ceratocystis

Ceratocystis is among the the 11 defined genera in the Ceratocystidaceae family (De Beer et al. 2014, 2017; Mayers et al. 2015), comprising of 39 species (Marin-Felix et al. 2017; Barnes et al. 2003; Liu et al. 2018). These fungi typically produce black, globose ascomatal bases with long, elongated necks terminating in an ostiole, through which sticky hat-shaped ascospores exude (Lowy 1982; Seifert et al. 1993). Phylogenetic analysis revealed four clades based on geographical distribution, including the Latin American clade (LAC), the North American clade (NAC) (Johnson et al. 2005), the African clade (AFC) (Heath et al. 2009; Mbenoun et al. 2014) and the Asian-Australian clade (AAC) (Harrington 2000; Engelbrecht and Harrington 2004; Johnson et al. 2005; Thorpe et al. 2005; Li et al. 2017). The LAC clade includes species associated with diseases affecting shisham-growing regions.

Type species: Ceratocystis fimbriata (Ellis & Halsted)

C. fimbriata is classified as follows: domain Eukaryota, kingdom Fungi, phylum Ascomycota, class Sordariomycetes, order Microascales, family Ceratocystidaceae, genus Ceratocystis, and species fimbriata. This species has undergone extensive taxonomic revision, initially reported from sweet potato (Harrington 2000; De Beer et al. 2014; Halsted 1890). Later, the species was transferred to Sphaeronaema by Saccardo (1892), to Ceratostomella by Elliott (1923), to Ophiostoma by Melin and Nannfeldt (1934), to Endoconidiophora by Davidson (1935), and finally to Ceratocystis by Bakshi (1950). In the past few decades, species identification in the genus Ceratocystis has continued to be a challenge for taxonomists, but with the help of molecular tools, many of these complexities have been resolved. C. fimbriata is a complex cryptic species that has a unique host range and geographic distribution.

Ceratocystis species involved in hardwood tree decline

Ceratocystis has a broad host range and is a wound-invading pathogen of woody plants (Tarigan et al. 2011; CABI 2021b). Diseases caused by Ceratocystis have been frequently reported to cause cankers, declines, diebacks, and vascular wilts in trees (Table 1) (Kile 1993; Marin Montoya and Wingfield 2006; Roux and Wingfield 2009). The fungus has been reported on six continents on various hosts with varying levels of virulence (Alizadeh et al. 2024). The rise of new tree diseases caused by Ceratocystis spp. has led to increased concern (Ploetz et al. 2013; Tsopelas et al. 2017).

Table 1 Diseases caused by C. fimbriata on woody hosts and their distribution

Disease management: options and challenges

C. fimbriata was reported a decade ago as a leading cause of shisham dieback, wilt, and decline in Pakistan (Al Adawi et al. 2009; Poussio et al. 2010; Latif et al. 2023). Given the increasing impact of shisham dieback caused by Ceratocystis spp., there is an urgent need to understand the nexus of host‒ interactions and the scope of existing disease management options to mitigate the impact of the fungus. At present, there are limited published guidelines for Ceratocystis management in shisham. Although some researchers have discussed managing shisham dieback by identifying host resistance genes or chemical controls, designing adequate control and management measures to levels deemed acceptable requires a long-term commitment, and the need to protect the host for several decades is a challenging prospect. Options for managing diseases such as oak wilt, eucalyptus wilt, and mango decline caused by Ceratocystis spp., however, may provide a baseline management approach for shisham dieback. As research progresses, management tactics for shisham will be refined.

In vitro chemical management of Ceratocystis spp.

Propiconazole (88.88%), difenoconazole (84.75%), hexaconazole (81.11%), and benzimidazole (77.73%) were found to be effective in in vitro tests against Ceratocystis dalbergicans. However, a decrease in the efficacy of these fungicides was observed in greenhouse trials on shisham seedlings, while these fungicides proved ineffective in preventing complete tree loss (Latif et al. 2023). Fungicides, including propiconazole (100%), hexaconazole (94.65%), difenoconazole (85.70%), thiram (74.35%), and copper oxychloride (70.52%), have shown considerable efficacy against C. fimbriata (Khan et al. 2017). Fungicides such as captan, carbendazim, hexaconazole, propiconazole, mancozeb, and chemicals, such as boric acid, completely inhibit C. fimbriata growth under controlled conditions (Sharma et al. 2010). A strong inhibitory effect on the mycelial growth of C. fimbriata was obtained by applying difenoconazole, thiabendazole, and fluazinam (Scruggs et al. 2017). Yang et al. (2000) reported high inhibition of C. fimbriata by thiophanate-methyl, carbendazim, and liguoling. As much as 4.34% mean diameter of inhibition of C. manginecans was achieved using Lanomyl 680 WP, Ao'yo 300SC, Carbenzim 500FL, and Ridomil Gold 68 WG fungicides (Tran et al. 2018).

In vivo management of Ceratocystis spp.

There are some reports on the rapid detection of Ceratocystis spp. from air, soil, and plant samples using real-time PCR assays, which have practical applications and can effectively be used to detect the pathogen in asymptomatic plants at much earlier stages, allowing sufficient time for the development of management practices to mitigate disease (Dharmaraj et al. 2022; Heller et al. 2023). A field study was conducted on twenty-four 3-year-old shisham trees inoculated with C. dalbergican to evaluate the field efficacy of propiconazole and difenoconazole. Researchers have concluded that although these fungicides cannot control tree death, they could considerably help to minimize disease severity (Latif et al. 2023). Oak wilt can be managed by intravascular injections of systemic triazole compounds, e.g., propiconazole (Juzwik et al. 2011). Compared with untreated controls, container-grown live oaks treated with propiconazole exhibited decreased disease severity and fewer diseased trees. The crown loss in naturally infected live oak plants treated with propiconazole (0–41%) was lower than that in nontreated (61–100%) plots. Furthermore, intravascular tree injection provided better disease control at the presymptomatic or preventive stage (Appel 1992). Propiconazole does not eliminate C. fagacearum from infected trees. However, preventive propiconazole treatments delay symptom development and tree mortality for at least two years in treated trees (Wilson 2005; Blaedow 2009; O’Brien 2011). Blaedow et al. (2010) reported that the efficacy of propiconazole decreased by up to 69% after two years due to chemical degradation in plant roots and lower stems. Soil drenching with carbendazim or propiconazole + chlorpyriphos was shown to be effective for the in-field management of Ceratocystis wilt in pomegranate (Sharma et al. 2010). Researchers in California tested the efficacy of Arbotect 20-S (thiabendazole) trunk injections in controlling C. fimbriata f. sp. platani, causing canker stain in Platanus acerifolia (Perry et al. 1988). These researchers found that Arbotect 20-S provided satisfactory control of the targeted pathogen.

Plant resistance as a powerful tool for managing Ceratocystis-induced diseases

Plant protection, especially from fungal pathogens, is commonly achieved by resistance breeding (Vale et al. 2001). The best strategy for disease control is planting resistant hosts (Oliveira et al. 2016). The use of resistant germplasm is the most feasible disease control option for plantation forests (Tarigan et al. 2016). In many cases, resistance can be a more effective and sustainable tool than any other IDM strategy for managing forest diseases, including diseases caused by Ceratocystis (Vale et al. 2001; Wingfield et al. 2001; Harrington 2013).

Plant resistance to C. fimbriata in woody hosts

Shisham

Genetic factors involved in shisham dieback resistance were explored by studying the NBS-LRR gene family. Transcriptomic analyses of Ceratocystis-inoculated shisham plants were conducted using DOP-rtPCR. Physiochemical characterization, subcellular localization, predicted protein fingerprints, in silico functional annotation, and structural modeling of identified resistance gene analogs (RGAs) suggested potential efficacy against microbial pathogens (Ijaz et al. 2022). The effects of RGAs on Ceratocystis-induced tree dieback in shisham were investigated by Ijaz and colleagues (2023a). They predicted that Ds-DbRCaG-02-Rga.a, Ds-DbRCaG-04-Rga.b, and Ds-DbRCaG-06-Rga.c might have contributed to the regulation of the immune response in shisham. Ijaz et al. (2023b) investigated the in silico characterization of short-nucleotide sequences. These short RGAs have been shown to play a role in stress and disease resistance.

Eucalyptus

In Brazil, 37 different four-month-old eucalyptus clones were tested for resistance to Ceratocystis wilt. The clones displayed a range of resistance, with most showing moderate resistance, while only one exhibited susceptibility (Tumura et al. 2012). Variation in resistance ranging from highly susceptible to highly resistant between genotypes of both E. grandis and E. urophylla to Ceratocystis wilt was observed in stem inoculation studies. Of the 21 parents tested, nine were susceptible, and 12 were resistant (Rosado et al. 2010). Similarly, researchers have shown that various Eucalyptus species are resistant to C. fimbriata (Mafia et al. 2011). In another study, eighteen commercial clones of hybrid eucalyptus (E. grandis × E. urophylla) were artificially inoculated with isolates of C. fimbriata to identify resistance genes. Six clones were highly susceptible, eight were moderately susceptible, and four were resistant, showing no discoloration on inoculated stems (Zauza et al. 2004). Five out of 20 eucalyptus genotypes showed resistance to different isolates of Ceratocystis (Firmino et al. 2013).

Mango

Utilizing host resistance is a common approach for managing mango wilt. In Brazil, the mango cultivars Espada, Haden, and Palmer, which were artificially inoculated with C. fimbriata, exhibited greater susceptibility, whereas the cultivars Tommy and Uba exhibited moderate to complete resistance (Araujo et al. 2014). In another study, five mango cultivars were inoculated with C. fimbriata isolates. Significant differences in cultivar vs. isolate interactions were recorded. The 'Uba' cultivar showed the highest resistance levels, regardless of the Ceratocystis isolate it was challenged with (Oliveira et al. 2016). Eight-year-old mango trees from 15 different cultivars grown in the field were subjected to pathogen challenge with two different isolates of C. fimbriata (highly pathogenic and nonpathogenic). Four varieties (Van Dyke, Edwards, Irwin, and Sao Quirino) were resistant, one (IAC 100 Bourbon) was moderately resistant, five (Glenn, Joe Welch, Zill, and Haden) were susceptible, and two (Kent and Jasmin) were resistant to one isolate but susceptible to the other (Rossetto et al. 1996). The inheritance of resistance to C. fimbriata was studied by artificially inoculating commercial mango varieties. The experiment concluded that inheritance is polygenic, with greater dominance effects and possible involvement of epistatic interactions. A low frequency of alleles favorable to disease resistance was observed. In addition, a 46% reduction in disease severity was observed. The results revealed that the Keitt, Palmer, Tommy Atkins, and Van Dyke cultivars were moderately resistant, whereas the Coquinho, Espada, and Haden cultivars were susceptible (Arriel et al. 2016).

Other hosts

In Brazil, screening of kiwifruit cultivars identified 'Bruno' and 'Chieftain' as resistant, while Actinidia arguta and 'Ken's Red' were highly susceptible to C. fimbriata infection (Alfenas et al. 2017). Host plant resistance to C. fimbriata has also been used to successfully control disease in Citrus (Paez and Castano 2001), Coffea (Castro Caicedo et al. 2013), Cocoa (Nunez et al. 1992) and poplar (Przybyl 1984) plants.

Conclusions

This review highlights three key points:: (1) shisham dieback is widespread in both native and nonnative regions; (2) it is predominantly caused by fungal pathogens, with abiotic factors possibly influencing symptom severity; and (3) current management guidelines are limited and insufficient as a comprehensive strategy.

Shisham dieback has become a textbook example of one of the most destructive and widespread diseases. It has been estimated that billions of mature shisham trees have been destroyed by outbreaks of this disease in Bangladesh, India, Pakistan, and Nepal within 100 years. Shisham dieback disease is usually described as a complex pathosystem that involves complex interactions among several biotic and abiotic factors. Abiotic factors can influence the development of symptoms in diseased trees.

Several studies have been conducted on shisham dieback, but most have reported conflicting results. Many questions remain unanswered about the key aspects of shisham dieback: is this disease truly a dieback, or is it a decline or wilt? What is causing it? Abiotic factors or biotic factors? Could it be caused by more than one organism? Finding answers to these questions is critical: it is impossible to inform management strategies without an understanding of these key disease features.

Several information gaps and scientific uncertainties limit the conclusions that can be drawn about trends in shisham mortality. Several researchers are unable to determine whether biotic or abiotic stresses are triggering factors. They differ in terms of their knowledge level, expertise in isolating fungi, and pathological background. Some researchers misunderstood and tried to make the correlation that abiotic factors might have contributed to this disease because shisham is a tropical species that demand high amounts of water and good drainage. Therefore, plants are vulnerable to acute drought or waterlogged conditions that can damage roots and attract different weak fungal pathogens. They also reported that shisham stands did not show any mortality in the Besham, Himalayan valleys (Fig. 5), one of the regions known as the center of shisham origin. In contrast, many scientists have established that shisham dieback is also present in Besham (Fig. 5), caused mainly by fungal pathogen(s), and some predisposing factors can accelerate this disease. Forest fungal pathogens, especially Ceratocystis species, are usually more aggressive under stressful conditions such as drought and rainfall. Furthermore, environmental variables can enhance or decrease pathogen(s) activity. Moreover, a closely related species, Ophiostoma ulmi (formerly known as Ceratocystis ulmi), likely originated in Asia near the foothills of the Himalayan Mountains. This supports evidence suggesting that both the host, shisham, and the pathogen, Ceratocystis, may also have originated in the Himalayan valleys, remaining undetected until recently.

Fig. 5

Surveys and sampling in the Himalayan region of Pakistan. a, b healthy shisham plantation along the Sindh River in Basham, KPK. c, d collection of wood samples from the stem portion of infected shisham trees. Photo credits: All the pictures by Muhammad Zunair Latif, except a by Javed et al. (2023b)

Ceratocystis can only be found in published research from the last decade linked to shisham dieback, suggesting that the pathogen has a relatively recent history with shisham hosts. There is a clear association between Ceratocystis and dieback symptoms in shisham, and C. dalbergican has been established as the causal organism. Previously, Fusarium was linked to wilt/dieback disease in Shisham. This disease has been differentiated from often-confusing Fusarium wilt on the same plant and explains dieback, a separate disease of shisham (Latif et al. 2023; Ul Haq et al. 2023).

At present, there are limited published guidelines for Ceratocystis management in shisham. Chemicals, such as propiconazole, difenoconazole, hexaconazole, thiabendazole, and benzimidazole, have yielded valuable results in the laboratory but are not as promising in greenhouse/field trials. Molecular studies have identified resistance gene analogs (RGAs), Ds-DbRCaG-02-Rga.a, Ds-DbRCaG-04-Rga.b, and Ds-DbRCaG-06-Rga.c. These short RGAs play a role in stress and disease resistance in shisham. These management options have been evaluated on a limited scale and can only help provide baseline information, but they can not be considered a solid management plan to mitigate this disease.

While researchers have explored potential management strategies, including identifying host resistance genes and chemical control methods, achieving sustainable disease control will require long-term, dedicated efforts due to the extended lifespan of shisham trees. Hopefully, fast-evolving technologies and advances in data analysis will soon lead to breakthroughs in our understanding of this complex pathosystem and in ways in which we can improve the resistance of susceptible host germplasm.

We hope this literature review will provide a scientific consensus regarding the name and etiology of the disease. Future research must emphasize (1) developing rapid detection tools to identify disease at early stages so that tree loss can be minimized and (2) identifying and propagating resistant trees for the sustainable production of shisham.