Abstract
Vegetative propagation in sugarcane favours accumulation of pathogens inside the canes and carryover of pathogenic inoculum through planting materials. Except foliar diseases, disease-infected setts serve as a primary source for disease spread for most of the diseases in the crop. In case of fungal diseases, planting infected setts leads to disease builds up in plant crop and probably death of the affected clump. However, in case of non-fungal diseases continuous accumulation of pathogens systemically leads to loss of vigour in sugarcane varieties referred to as ‘varietal degeneration’ and this results in loss of yield potential in elite commercial varieties. Past decades witnessed many such instances of degeneration in popular sugarcane varieties and their replacement with new varieties. With the development of precise molecular diagnostic tools, the associated pathogens were precisely identified. Under Indian conditions, it was found that combined or separate infections of viruses causing mosaic and yellow leaf (YL), phytoplasmas causing grassy shoot and leaf yellows and bacterium causing ratoon stunting disease are associated with varietal degeneration. The degeneration was rapid and severe when all these pathogens infect sugarcane together as compared to their separate infections. However, among all these diseases, YL contributes more towards degeneration of sugarcane varieties. The disease occurrence to epidemic levels in different states is a serious concern for sugar industry and due to that longevity of the affected varieties in the field is threatened. Meristem-tip culture combined with molecular diagnosis was found effective eliminate the pathogens efficiently from the cane. Developing disease-free nurseries is imperative to sustain productivity of sugarcane and to realize yield potential of popular sugarcane varieties in India.
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Introduction
More than 50 diseases caused by fungi, bacteria, virus, phytoplasma and nematode are reported to infect sugarcane in India and other countries (Rao et al. 2002; Rott et al. 2000). Red rot caused by Colletotrichum falcatum had been a serious threat to sugarcane cultivation in the Subcontinent for the more than a century and it is responsible for the elimination of many commercial varieties (Viswanathan 2010). During each epidemic, the crop was saved by releasing new varieties with red rot resistance. Although the efforts were continued, the pathogen remained dominant and determined varieties under cultivation in the red rot endemic areas of subtropical plains, East Coast regions and Gujarat. Although other fungal diseases like smut and wilt were not destructive as like red rot they have also played a decisive role in varietal selection for cultivation in certain regions. The diseases caused by viruses, bacteria and phytoplasmas were never considered as threats to sugarcane cultivation in the country.
However, these non-fungal pathogens associated with yellow leaf (YL), mosaic, grassy shoot and ratoon stunting disease (RSD) systemically infect sugarcane. Over the years, such systemic accumulation of these pathogens reduces cane and sugar yield. In contrast to fungal diseases, where very severe losses to crop yield are expected in the field, these non-fungal pathogens in sugarcane causes gradual decline in varietal performance. Although these viral/bacterial pathogens cause limited symptoms in the field, continuous vegetative propagation results in enhanced pathogen titre that would increase the pathogenic potential to cause severe symptoms. Combined infection of viral/bacterial/phytoplasmal pathogens accelerates the damage to the crop and this is due to infection of one pathogen making the plant more susceptible to another. In this way, a variety degenerates faster and its potential comes down in the field after some years in the field. This phenomenon is referred to as ‘varietal degeneration’ in sugarcane (Viswanathan and Padmanaban 2008). The popular cv Co 419 degenerated in the past due its high susceptibility to mosaic, YL and RSD in Karnataka state. Similarly the popular varieties of the tropical region Co 740 and CoC 671 degenerated due to their high susceptibility to mosaic and YL in different parts of Karnataka and Maharashtra. The cv Co 86032 has replaced them in large areas in these states due to their degeneration. The review analyses the factors contributing to varietal degeneration in sugarcane due to non-fungal diseases, their diagnosis and management.
Spectrum of Virus(es) Infection in Sugarcane
YL caused by Sugarcane yellow leaf virus (SCYLV) and mosaic caused by Sugarcane mosaic virus (SCMV) and Sugarcane streak mosaic virus (SCSMV) are the major viral diseases in India. Detailed studies were taken up on the prevalence of these viruses in varieties originated from 11 different states in the country through RT-PCR revealed that 93.44 % of varieties were infected with SCSMV, 31.15 % with SCMV and 27.87 % with SCYLV. Of the 61 varieties, 47.5 % were infected with SCSMV alone, 3.28 % with SCMV alone and 4.92 % with SCYLV alone. However, 21.3 % of them had combined infections of SCSMV and SCMV and similarly 16.4 % of them had combined infections of SCSMV and SCYLV. About 6.5 % had mixed infections of all the three viruses. Overall, the assay results indicated that SCSMV is predominant among the three viruses and it has been found as a major causative virus of sugarcane mosaic (Viswanathan and Karuppaiah 2010). This study also revealed extensive spread of these viruses in sugarcane varieties and practically none of them is free from any of the viruses. Leaf fleck caused by Sugarcane bacilliform virus (SCBV) is a lesser known disease of sugarcane in India. Recent PCR assays with 28 samples for SCBV revealed that the virus is amplified in 75.0 % of the samples. Among them 89.5 % were commercial cultivars, which revealed that majority of the varieties under cultivation, having the virus infection (Viswanathan and Rao 2011). Although impact of this virus on sugarcane growth was not established, its widespread occurrence in the field suggests that it may become a threat in future years.
Impact of Yellow Leaf on Sugarcane
Earlier studies conducted at Sugarcane Breeding Institute (SBI), Coimbatore indicated that drastic reduction in number of millable canes in sugarcane cvs Co 6511, Co 86032, CoS 687 and CoV 92101 due to SCYLV infection (Viswanathan et al. 2006). Previously, Viswanathan (2002) showed that the disease infection results in reduction in cane diameter and photosynthetic rate in most of the affected varieties. However, the reduction was significant in cvs CoS 510, CoS 767, CoS 8407 and Co 775. In endemic locations of South India such as Tamil Nadu, Karnataka and Andhra Pradesh diseased canes recorded 37.23 % reduction in cane weight, 15.25 % in diameter, 5.03 % in intermodal length and 19.45 % in juice yield from cane (Viswanathan and Rao 2011).
Recent studies of Viswanathan et al. (2014) assessed physiological parameters in symptomatic and asymptomatic plants of 10 different cultivars and a genotype and established that among several physiological parameters, photosynthetic rate, stomatal conductance and SPAD meter values were significantly reduced in cultivars severely infected with SCYLV. Virus-infected varieties recorded significant reductions in growth/yield parameters, such as stalk height, stalk thickness and number of internodes. In addition to reductions in stalk weight, height and girth, SCYLV infection also reduced juice yield in the affected canes up to 34.15 %.
Under field conditions, the major impact on YL infection was found on cane thickness and height in sugarcane. Fresh weights of comparable internodes of the infected plants are only 20–65 % of the weight of healthy plants. It is estimated that severe infection of the virus reduces cane yield by 30–50 % and sugar recovery is reduced significantly in the mills (Viswanathan 2012a). Since the loss caused by the disease is phenomenal in the field as well as in the mills, both the cane growers and millers suffer due to the disease.
Globally impact of the disease on sugarcane growth and yield has been well documented. SCYLV-infected asymptomatic plants showed CO2 assimilation rates and stomatal conductance 10–30 % lower than healthy plants, and water relations resembled those of salinity- and drought-stressed plants (Lehrer and Komor 2009). In addition, reductions were found in the contents of photosynthetic leaf pigments and in the chlorophyll a/b ratio (Gonçalves et al. 2005) along with ultrastructural changes in Krans cell chloroplasts (Yan et al. 2009). Carbohydrate content in the leaves also increased as a secondary effect of the SCYLV infection, suggesting a reduction of assimilate export in infected plants. The virus affects total reducing sugars, leaf areas and chlorophyll content and sugar transport (Fontaniella et al. 2003, Izaguirre-Mayoral et al. 2002; Gonçalves et al. 2005, Lehrer et al. 2007). Overall, asymptomatic plants suffer a yield decline of 10–30 % depending on cultivar and ratoon cycle (Lehrer et al. 2007; Grisham et al. 2009; Rassaby et al. 2003).
Although the disease was there in different parts of India for more than 10 years, its prevalence are ignored probably due to leaf mid rib yellowing is thought to be a phenotypic character in leaves. The epidemic occurrence of the disease has taken a toll on many varieties without being noticed by the concerned people that the poor performance of the varieties is due to YL. In ratoon crop, the intensity of the disease will be much higher than in plant crop. However, when SCYLV-infected planting materials are used for planting, the disease expresses in the plant crop and the disease severity in ratoons will be much more than expected.
Impact of Mosaic
In India, the presence of this disease in sugarcane was first authenticated by Barber (1921), since then its widespread occurrence was reported from all the sugarcane growing tracts in the country. Despite, mosaic is not a major problem in some countries; it has caused substantial yield losses in other countries by severe outbreaks of the disease (Koike and Gillaspie 1989). Advancements made in diagnosis of the viruses through serological and molecular techniques led to precise diagnosis of the virus(es) and established the losses with more assurance and authority. Koike and Gillaspie (1989) observed that the yield loss due to mosaic does more pronounced as the virus/viral strains remains in infected cane for generations which leads to decline in cane yield and sucrose content. Varietal degeneration due to mosaic is a serious concern that results in near extinction of elite cultivars from cultivation as witnessed to the erstwhile ruling varieties in the tropical region (Viswanathan and Balamuralikrishnan 2005) and in the subtropical region (Singh et al. 2003) in India.
Agnihotri (1996) reported that SCMV causes an appreciable damage in susceptible varieties and even 10–15 % yield loss due to this disease is highly significant because of extensive cultivation of the crop. Virus infection significantly reduced the net CO2 assimilation rate during the grand growth period. At harvest, cane stalks from virus-infected plots recorded a significant reduction in cane diameter, cane weight and number of internodes. Results of juice analysis revealed that virus infection reduced brix, sucrose per cent, purity and commercial cane sugar per cent in both sugarcane cvs Co 740 and CoC 671. Overall, the study has established a clear impact of mosaic on sugarcane growth and yield in the popular varieties (Viswanathan and Balamuralikrishnan 2005).
Combined Infections of RSD and Sugarcane Viruses
The RSD pathogen colonies xylem vessels which conducts water and minerals from root to leaves when bacterial colonization increases inside the vessels, the sap movement is restricted. Similarly SCYLV colonizes sieve tube elements systemically affecting movement of photosynthates from leaves to other tissues. Such impairment in vascular system directly affects various metabolic processes, photosynthesis and transpiration in the plant. Although the pathogen does not affect these processes directly, its effect on water/nutrient movement to various tissues indirectly cause moderate to severe impairment to plant growth and metabolism when sugarcane is infected either by SCYLV or bacterium, severe impact on cane growth and yield is expected. Such combined infections cause comparatively more severe impact on plant growth and development (Viswanathan 2004a). This type of varietal degeneration due to combined infections of more pathogens was demonstrated in many varieties by comparing the growth in disease free and disease infected planting materials.
Agnihotri (1990) observed that a synergy between SCMV and RSD also exists and greater losses are incurred when sugarcane is infected with both the pathogens simultaneously than their separate infections. Since occurrence of YL was not known that time it may be difficult to relate its association with varietal degeneration recorded before 1990s. Decline in varietal performance over the years in the popular varieties is mainly due to accumulated pathogens inside the stalk, affecting cane growth and photosynthetic efficiency, which directly results in reduced cane yield and sugar yield. Although these viral/bacterial pathogens cause limited symptoms in the field, continuous vegetative propagation results in enhanced pathogen load that would increase the pathogenic potential to cause disease. Combined infection of two or more viral/bacterial pathogens accelerates the damage to the crop in the field and this is due to infection of one pathogen makes the plant more susceptible to another. In this way, a variety degenerates faster and its potential comes down over the years.
Phytoplasmas Diseases in Sugarcane
Many phytoplasma diseases infecting sugarcane such as grassy shoot, white leaf, green grassy shoot and leaf yellows were reported worldwide (Rott et al. 2000). Of them, grassy shoot caused by sugarcane grassy shoot (SCGS) phytoplasma has been reported to cause severe impact on cane growth and yield throughout the country. Very high yield losses due to grassy shoot were reported in India for many years (Viswanathan 2000, Viswanathan and Rao 2011). Ratoon crops always record severe symptoms of the disease with more impact due to increase in pathogen load. Studies conducted at SBI showed that phytoplasma infection can cause 35 % reduction in stalk height, 15 % reduction in stalk girth, 50–60 % reduction in length of internodes. Above all 50–75 % plant crop infection resulted in 100 % failure in millable cane production in the ratoon crop of a clone ISH 152 (Viswanathan 2000). Recently Kumar et al. (2015) provided a clear evidence on the association of 16SrI-B subgroup phytoplasma associated with Sugarcane leaf yellows in the country. The disease has been reported in a severe form on the popular varieties CoLk 94184 and CoSe 92423 in Uttar Pradesh. Since YL and leaf yellows cause almost similar symptoms in sugarcane there could be combined infections of SCYLV and leaf yellows phytoplasma in sugarcane. Further studies are required to delineate symptoms caused by both the pathogens in sugarcane and to assess impact to sugarcane in combined infections.
Diagnosis of Sugarcane Pathogens Through Serological and Molecular Techniques
In the past, ELISA has been extensively used for the diagnosis of Leifsonia xyli subsp xyli (Lxx) causing RSD in sugarcane (Viswanathan 1997, 2001). Further, sensitivity of ELISA was compared with dot-blot and tissue blot assays and the results revealed that ELISA and tissue blot were equally effective it detecting Lxx and were more efficient than dot blot (Data not shown). Several variations in serological techniques were developed and used in different countries to develop RSD-free planting materials (Bailey and Tough 1992, Croft et al. 1994, Hoy et al. 1999, Viswanathan 2004b, Young and Brumbley 2004). PCR assays were also developed for Lxx diagnosis in sugarcane (Fegan et al. 1998; Taylor et al. 2003). Although PCR technique is more sensitive, inhibitors found in the sap continue to limit its sensitivity (Grisham 2004). Association of the virus with YL was established through DAS-ELISA technique at SBI, Coimbatore (Viswanathan 2002; Viswanathan and Balamuralikrishnan 2004). Later RT-PCR techniques were found to be more sensitive to detect SCYLV before symptom expression and in tissue culture raised plants (Viswanathan et al. 2008a, 2009). Assays were also developed to detect more than one virus in a reaction through duplex and multiplex-RT-PCRs (Viswanathan et al. 2008b, 2010, Xie et al. 2009). In addition to the viruses, PCR assays were developed to detect phytoplasmas associated with grassy shoot and leaf yellows (Rao et al. 2008, 2012, 2014; Kumar et al. 2015; Viswanathan et al. 2005).
Management of Varietal Degeneration in Sugarcane
In sugarcane, disease resistance has been successfully exploited to manage major fungal diseases such as red rot, smut and wilt in India and other South Asian countries. However, there is no systematic breeding or screening programme to develop resistance to grassy shoot, RSD, YL and mosaic of sugarcane in these regions. Addition of new selection traits will complicate varietal selection process in the current varietal developmental programme and also the process will become more cumbersome. The diseases associated with varietal degeneration can be managed successfully through healthy seed nursery programme whereas this approach is not sufficient to manage fungal diseases in the crop. Hence three-tier seed nursery programme was advocated to manage non-fungal diseases of sugarcane such as grassy shoot and RSD during the last 3–4 decades in the country (Viswanathan 2013; Viswanathan and Rao 2011). Heat therapy, either aerated steam or moist hot air was employed to inactivate grassy shoot phytoplasma/Lxx in seed canes in this programme. Partial or complete inactivation of these pathogens was adequate to manage these two important diseases contributing towards varietal degeneration in a 5 year seed cycle. Since heat therapy is ineffective against viral diseases, tissue culture methods were employed to eliminate systemic virus(es) infection in sugarcane in different countries.
Meristem culture has been exploited for the production of virus-free plants by meristem culture in many vegetatively propagated crops. By this approach, it has been possible to eliminate SCYLV and other viruses from many sugarcane commercial varieties worldwide. Ever since YL became a serious constraint to sugarcane production in different countries efforts were made to manage the disease through different strategies. Among the different approaches, going for meristem culture technique was found to be more effective in the elimination of the causative virus from the systemically infected plants (Ramgareeb et al. 2010, Snyman et al. 2011). At our conditions incorporation of nucleic acid analogues like ribavirin improved the efficiency of SCYLV elimination from the infected mother plants. Since these virus elimination techniques are not 100 % efficient to eliminate the virus there is a need to index the sugarcane seedlings using precise techniques. At seedling stage, the disease symptoms are not expressed. Also symptom expression in meristem derived plants in the field may be suppressed due to very low titre of the infective pathogens. Many improved diagnostic techniques based on serological and molecular techniques were developed to detect these pathogens. Meristem culture combined with molecular diagnosis was proved to be successful to effectively manage the disease. Detailed studies conducted at SBI proved that SCYLV elimination can be achieved through meristem culture combined with molecular diagnosis. The virus-free plants have maintained a good crop stand under field conditions and recorded higher yield than the conventional seed planted fields (Viswanathan 2012b). Earlier Chatenet et al. (2001) and Parmessur et al. (2002) reported successful elimination of SCYLV by tissue culture from infected sugarcane plants from France and Mauritius, respectively.
The potential for eradicating pathogens via rapid regeneration of plants directly from leaf roll discs was explored in South Africa. The technique, NovaCane®, has been used successfully to remove SCYLV (Snyman et al. 2008). In addition, this process enabled elimination of bacterial pathogens from diseased sugarcane plants while simultaneously enabling large-scale micro propagation. Cheong et al. (2012) developed procedures for the in vitro elimination of SCMV, Sorghum mosaic virus (SrMV), SCSMV, SCYLV and Fiji disease virus (FDV) from infected sugarcane and they standardized in vitro shoot regeneration, elongation and virus elimination through meristem tissue culture originating from both apical and axillary shoots and found 61–92 % virus-freedom among elongated shoots. Overall, clean seed programme initiated through tissue culture benefit sugar industry in different sugarcane growing countries.
Conclusion
Cane productivity remained static over the last five decades in India. Although newly introduced varieties were superior in yield and quality, under field conditions we could not harness the improved potential of yield and quality. The major reason for this situation is attributed to slow degeneration of the new varieties due to systemic accumulation of non-fungal pathogens in the canes. By the time the new variety becomes popular, it succumbs to different stages of degeneration depending on seed replacement programmes. The varietal degeneration was not recognized in the country till YL reached an epidemic level across the states. The crop loses about 2–3 months of its active growth depending on the pathogen load and plant or ratoon crop. The overall loss caused by YL and other pathogens associated with varietal degeneration could be several billion rupees in India, hence a clean seed programme is recommended to tackle this constraint. Adoption of disease-free nurseries raised from tissue (meristem) culture combined with molecular diagnosis resulted in a significant improvement in cane yield. In the long run, adopting disease-free nurseries will lead to enhanced cane productivity in the country and the elite commercial varieties will have an extended life with vigour.
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The author is grateful to Dr. N. V. Nair, former Director of the Institute for providing facilities and encouragement.
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Viswanathan, R. Varietal Degeneration in Sugarcane and its Management in India. Sugar Tech 18, 1–7 (2016). https://doi.org/10.1007/s12355-015-0369-y
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DOI: https://doi.org/10.1007/s12355-015-0369-y