Evaluation of BC1 and BC2 from the crossing Erianthus arundinaceus with Saccharum for resistance to sugarcane smut caused by Sporisorium scitamineum

RESEARCH ARTICLE

Evaluation of BC1 and BC2 from the crossing Erianthus arundinaceus with Saccharum for resistance to sugarcane smut caused by Sporisorium scitamineum

Wan-Kuan Shen^I; Hai-Hua Deng^II; Qi-Wei Li^II; Zhan-Duan Yang^II; Zi-De Jiang^III

^ICollege of Agronomy, South China Agricultural University/Scientific Observing and Experimental Station of Crop Cultivation in South China, Ministry of Agriculture, 510642, Guangdong, Guangzhou, China

^IIGuangzhou Sugarcane Industry Research Institute /Guangdong Key Laboratory of Sugarcane Improvement and Biorefinery, 510316, Guangdong, Guangzhou, China

^IIIDepartment of Plant Pathology, South China Agricultural University/Guangdong Key Laboratory of Microbial Signals and Disease Control, 510642, Guangdong, Guangzhou, China

^{Author for correspondence}

ABSTRACT

Sugarcane smut disease caused by the fungus Sporisorium scitamineum is one of the important fungal diseases affecting sugarcane yield and sucrose content around the world. Cultivar resistance is the most appropriate control method for this disease. In this study, 37 BC₁ lines chosen from the crossing YC96-40 (F₁ of Erianthus arundinaceus) × CP84-1198 (commercial sugarcane cultivar) and 42 BC₂ lines chosen from the crossing YCE01-116 (BC₁ of E. arundinaceus) × Neijiang57-416 (commercial sugarcane cultivar) were evaluated for smut resistance using artificial inoculation. The results showed that of 79 tested BC₁ and BC₂ lines of E. arundinaceus, 10 (12.7%) were highly to moderately resistant to smut. BC₁ of E. arundinaceus had more resistant lines than BC₂ of E. arundinaceus. Of the 37 tested BC₁ lines of E. arundinaceus, seven (18.9%) were highly to moderately resistant, while three (7.1%) of the 42 tested BC₂ lines of E. arundinaceus were highly to moderately resistant to smut. The resistant lines identified in this study could be used as sources of smut resistance in sugarcane breeding programs.

Key words:Erianthus arundinaceus, Saccharum officinarum, Sporisorium scitamineum, backcross progenies, evaluation of resistance.

INTRODUCTION

Sugarcane (Saccharum hybrid species) is an important economic crop for sugar and ethanol production. Mainland China is currently the third largest producer of sugarcane in the world, following Brazil and India. Southern China, including Guangxi Zhuang autonomous region, Yunnan and Guangdong Provinces, is the major sugarcaneproducing region in mainland China (Chen & Yuan, 2010). Sugarcane smut caused by the fungus Sporisorium scitamineum, formerly called Ustilago scitaminea (Stoll et al., 2003), is an important disease worldwide (Comstock, 2000). It was reported for the first time in the world in 1877 when it was found in Natal, South Africa (McMartin, 1945), and numerous outbreaks were noted in Africa and Asia in the following decades. Smut remained confined to the Eastern hemisphere until it was found in Argentina in 1940 (Comstock, 2000). In China, smut was found in 1932 in Guangzhou for the first time (Antoine, 1961; Presley, 1978). During the past 20 years, smut has developed into a major disease and caused serious yield loss in sugarcane production in mainland China (Que et al., 2012 ; Shen et al., 2013).

The most efficient and economic method for disease control, including sugarcane smut, is the use of resistant cultivars (Wada, 2003; Shen et al., 2014). However, the development of resistant sugarcane cultivars requires elite sources of resistance to smut. Modern sugarcane cultivars are derived from a relatively few interspecific hybrids between Saccharum officinarum L. and S. spontaneum L., resulting in a narrow germplasm base (Berding & Roach, 1987). To increase this restricted genetic base, breeders have been interested in the introgression of genes from wild species.

Erianthus arundinaceus is an important closely related wild species of S. officinarum. This species has great potential as a germplasm source for modifying the ratooning ability, vigour, tolerance to environmental stresses, and disease resistance of sugarcane (George et al., 2000; Fukuhara et al., 2013). E. arundinaceus was first hybridized with sugarcane in 1885 (Deng et al., 2004). However, further progress was not made until the 1990s, because of the sterility of hybrids and the difficulty in identifying genuine progenies (Shen, 2002). In recent years, great progress has been made in the use of E. arundinaceus, and some promising BC₁ and BC₂ lines have been obtained from crossing E. arundinaceus with Saccharum (Deng et al., 2004). Several studies on physiological and biochemical characteristics or chromosome transmission in backcross progenies of E. arundinaceus have been conducted (Chen et al., 2006; Deng et al., 2007; Deng et al., 2009). However, there have been no reports on the assessment of BC₁ and BC₂ of E. arundinaceus for resistance to sugarcane smut. The objective of this study was to evaluate smut resistance in BC₁ and BC₂ lines of E. arundinaceus.

MATERIALS AND METHODS

Materials and experimental site

Seventy-nine backcross progenies of E. arundinaceus, including 37 BC₁ lines and 42 BC₂ lines, and their parents, YC96-40 (F₁ of E. arundinaceus), CP84-1198 (commercial sugarcane cultivar), YCE01-116 (BC₁ of E. arundinaceus) and Neijiang57-416 (commercial sugarcane cultivar), were kindly provided by Hainan Sugarcane Hybridization Station, Guangzhou Sugarcane Industry Research Institute, Guangzhou, China. Seventy-nine BC₁ and BC₂ lines of E. arundinaceus, YC96-40 and YCE01-116 have been identified as true hybrids of E. arundinaceus by molecular approaches (He et al., 2008). This study was carried out in June of 2008 at Guangzhou Sugarcane Industry Research Institute, China.

Preparation of planting sets

Sugarcane stalks from a 7-month-old plantation were cut and the leaves dettached to expose the buds. These were then cut into one-budded setts ready for inoculation.

Inoculation and planting of prepared planting sets

For screening resistance in the field, teliospores of S. scitamineum were collected from mature unopened sori produced on canes in field at Zhanjiang sugarcane production areas, Guangdong Province, China. Spore germination was determined under a compound microscope (Olympus, Model BH-2) at 100× using a micro-counter as described by Bhuiyan et al. (2012). Two gram smut spores were mixed with one liter of distilled water as per standard screening practices (Shen & Deng, 2011). The spore suspension is prepared in a 50 liter tank giving a concentration of approximately 4-5 million spores per milliliter. One-budded sets of the tested BC₁, BC₂ lines of E. arundinaceus and their parents were dipped into smut spore suspension for 30 min as described by Shen and Deng (2011). The inoculated sets were then incubated in wet jute gunny bags overnight and planted in plastic buckets (35 cm diameter, 30 cm depth) filled with a steam-sterilized mixture of soil and organic matter (3:1 v/v). A total of 30 plants of each test material were treated according to a completely randomized experimental design including three replicates of individual bucket containing 10 plants. Plants were grown in greenhouse at 28-30 ºC.

Investigation of incidence and resistance classification

Approximately 4-5 weeks after inoculation, surveys of disease incidence were initiated and carried out every 15 days until the disease incidence was stable (six months). The date of inoculation, number of total stools, number of diseased stools were recorded. Disease reactions of the tested materials for S. scitamineum were rated on a scale from 1 to 9 based on the percentage of diseased stools (Shen et al., 2014), where 0-3% was scored as grade 1 (highly resistant), 4-6% as grade 2 (resistant), 7-9% as grade 3 (resistant), 10-12% as grade 4 (moderately resistant), 1325% as grade 5 (moderately susceptible), 26-35% as grade 6 (susceptible), 36-50% as grade 7 (susceptible), 51-75% as grade 8 (highly susceptible), and 76-100% as grade 9 (highly susceptible).

RESULTS

From a total of 79 BC₁ and BC₂ lines of E. arundinaceus, resistance to smut ranging from grade 1 (highly resistant ) to grade 4 (moderately resistant) was detected in 12.7% (10 out of 79) lines (Table 1). The percentage of resistant lines in BC₁ of E. arundinaceus (18.9%, seven out of 37) was higher than that of BC₂ (7.1%, three out of 42). In BC₁ of E. arundinaceus, five (13.5%) of the 37 tested BC₁ lines were highly resistant to smut. Resistant was found in 5.4% (two out of 37) of BC₁ lines, and 81.1% (30 out of 37) of BC₁ lines were susceptible to smut, ranging from grade 5 (moderately susceptible) to grade 9 (highly susceptible). Of the BC₂ lines of E. arundinaceus, one line was scored as highly resistant (grade 1), counting for 2.4% (1 out of 42), two lines exhibited resistance (grade 3) to smut, and 92.9% (39 out of 42) lines were susceptible to smut, ranging from grade 5 (moderately susceptible) to grade 9 (highly susceptible). The female parent YC96-40 (F₁ of E. arundinaceus) and the male parent CP84-1198 (commercial sugarcane cultivar) of BC₁ were both susceptible to smut, while the female parent YCE 01-116 (BC₁ of E. arundinaceus) and male parent Neijiang57-416 (commercial sugarcane cultivar) of BC₂ were both highly susceptible to smut.

DISCUSSION

In modern sugarcane breeding, the screening, identification and evaluation of systemic resistance in source materials is critical due to the importance of wild sugarcane resources as a source of resistance genes. Subsequent characterization and utilization of wild resistance genes can be used to broaden the genetic base of sugarcane resistance against disease and has important significance for screening and breeding of resistant cultivars (Li et al., 2013). Sugarcane smut has been the major sugarcane disease in mainland China in recent years. In this study, a total of 79 backcross progenies (BC₁ and BC₂) of E. arundinaceus were screened for resistance to smut using artificial inoculation method. Seven BC₁ and three BC₂ lines of E. arundinaceus were identified as highly to moderately resistant germplasms, which could provide an elite array of resistance sources for effective breeding of sugarcane cultivars against smut.

In this study, backcross progenies of E. arundinaceus with Saccharum showed no stronger resistance ability to smut, leading to only 18.9 % of BC₁ lines and 7.1% of BC₂ lines with highly to moderate resistance. The main reason was that the backcross progenies derived from susceptible crossings: BC₁ lines from a susceptible vs. susceptible crossing, and BC₂ lines from a highly susceptible vs. highly susceptible crossing. The heritability of sugarcane smut resistance is moderate (Wu et al., 1977, 1983; Comstock, 1983; Chao et al., 1990) therefore the resistance level of parental combinations affected the resistance ability of the offspring. On the other hand, BC₁ and BC₂ plants of E. arundinaceus have larger buds with smaller or no sprout wings, which are morphological features that may be beneficial to germination and infection of S. scitamineum (Muthusamay, 1974; Padmanaban et al., 1988a, 1988b) and thus may also have affected the resistance backcross progenies of E. arundinaceus to smut. Piperidis et al. (2010) reported that in the BC₁ lines of E. arundinaceus the number of chromosomes ranged from 21 to 30, while in the BC₂ lines the number ranged from 14 to 15, revealing cases of chromosome loss. Therefore, it is possible that resistance genes were lost in backcross progenies of E. arundinaceus, which may have lead to hybrid offspring without stronger resistance against smut.

In the future, further studies are needed to objectively evaluate the resistance ability of backcross progenies of E. arundinaceus to smut from resistant vs. resistant crossings or highly resistant vs. highly resistant crossings. It would be useful to get more promising resistance sources against sugarcane smut disease and reveal prospect of E. arundinaceus in breeding for resistance to smut.

In conclusion, this study has identified ten BC₁ and BC₂ lines of E. arundinaceus with resistance against sugarcane smut disease out of 79 tested lines, broadening the genetic basis of smut resistance in sugarcane breeding.

ACKNOWLEDGEMENTS

This work was supported by grants from the Earmarked Fund for Key Agriculture Project of Guangdong Province, China (2010B020302001) and the Earmarked Fund for President Project of South China Agricultural University, China (K13009).

Submitted: 25 January 2014

Revisions requested: 17 March 2014

Accepted: 19 May 2014

TPP-2014-0011

Section Editor: Rosana Rodrigues

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Publication Dates

• Publication in this collection
  31 Oct 2014
• Date of issue
  Oct 2014

History

• Received
  25 Jan 2014
• Accepted
  19 May 2014
• Reviewed
  17 Mar 2014