African Crop Science Journal, Vol. 6. No. 3, pp. 249-258,
ONTOGENETIC CHARACTERISTICS AND INHERITANCE OF RESISTANCE TO LEAF ANTHRACNOSE IN SORGHUM
A. TENKOUANO, F.R. MILLER1, R.A. FREDERICKSEN2 and R.L. NICHOLSON3
Department of Soil and Crop Sciences, Texas A&M University, College Station, TX 77843, USA
(Received 15 October, 1997; Accepted 7 July, 1998)
The objectives of this study were to understand the effects of ontogeny on the expression and inheritance of resistance of sorghum (Sorghum bicolor [L.] Moench) to Colletotrichum graminicola (Ces.)Wils., the causal agent of anthracnose. Two resistant cultivars (SC326-6 and SC599-11E) and two susceptible cultivars (BTx623 and B35-6) were inoculated in the greenhouse at different growth stages with three isolates of C. graminicola. The response of SC326-6 was hypersensitive while the reaction of SC599-11E was of a slow lesion delimitation type. Susceptible cultivars failed to restrict lesion growth, particularly in older plants. All cultivars produced phytoalexins in response to attempted infection, but synthesis of these antimicrobial compounds started earlier and proceeded faster in resistant cultivars. Field resistance to C. graminicola was expressed in both juvenile and adult plants of SC326-6 and its progeny. In contrast, reversal of resistance was observed in SC599-11E and its progeny as plant aged. The frequency distribution of disease severity indices was bimodal and fitted a 3:1 segregation, suggesting that resistance was controlled by dominance at a single multiallelic locus. The symbol cgl was proposed to designate the resistance locus.
Key Words: Colletotrichum graminicola, host plant resistance, ontogenetic interaction, phytoalexins, Sorghum bicolor
Les objectifs de cette étude étaient de comprendre les effets de l'ontogénie sur l'expression et la transmission génétique de la résistance du sorgho (Sorghum bicolor [L.] Moench) au Colletotrichum graminicola (Ces.)Wils., l'agent responsable de l'anthracnose. Deux cultivars résistants (SC326-6 and SC599-11E) et deux cultivars sensibles (BTx623 and B35-6) ont été inoculés en serre à différents stades de croissance avec trois isolats de C. graminicola. La réaction de SC326-6 a été hypersensitive alors que SC599-11E a plutôt freiné le développement des lésions. Les cultivars sensibles n'ont pu arréte la progression des lésions, notamment chez les plantes agées. Tous les cultivars ont secrété des phytoalexines en réponse à l'attaque, mais la synthèse de ces composés antimicrobiens a démarré plus tôt et a progressé plus rapidement chez les cultivars résistants. Au champ, la résistance à C. graminicola s'est exprimée autant chez les plantes juveniles qu'adultes du cultivar SC326-6 et de sa descendance. Par contre, on a observé un renversement de la résistance avec l'age chez le cultivar SC599-11E et sa descendance. La distribution de fréquence des indices de sévérité de la maladie était bimodale avec un ratio de 3:1, ce qui suggère que la résistance est sous contrôle d'un locus multiallélique unique. Le symbôle cgl est proposé pour désigner ce locus.
Mots Clés: Colletotrichum graminicola, résistance variétale, interaction ontogénétique, phytoalexines, Sorghum bicolor
Sorghum anthracnose is caused by Colletotrichum graminicola, a hemi-biotrophic fungus capable of attacking all aerial parts of the plant worldwide (Pande et al., 1991). Host plant resistance is considered the most economical and practical means of controlling anthracnose in sorghum (Warren, 1986). In this regard, genetic mechanisms that prevent the pathogen from becoming established within host tissues (Huang, 1986; Hoch and Staples, 1987; Gustafsson and Claesson, 1988) or from bringing its life cycle to completion (Tinline et al., 1989) would be the most useful for long term control of the disease, as this could reduce inoculum levels.
Juvenile plants of both genetically resistant and susceptible cultivars of sorghum are devoid of symptoms of anthracnose, but, as susceptible cultivars mature, they lose the ability to resist the pathogen (Ferreira and Warren, 1982; Nicholson et al., 1988). A similar pattern of anthracnose expression was reported for maize (Zea mays L.), which was attributed to a developmental change in host susceptibility (Nicholson et al. 1985; Jamil and Nicholson, 1987; Keller and Bergstrom, 1988).
Whether developmental changes in the host could regulate the phenotypic reaction of sorghum to attempted infection by the anthracnose fungus is not known. In particular, little has been reported on the initial events of the interaction between sorghum and C. graminicola and their relationship to expression of field resistance to the pathogen.
Analysis of resistance components has been found useful in the study of the resistance of plants to pathogenic fungi, especially the rusts and mildews (Parlevliet, 1979; Eening et al., 1982). Not only may resistance components be used to unravel the histological and physiological features of host-pathogen interactions (Baayen and van der Plas, 1992) but also appealing, and of greater practical interest, is the potential for their use as early criteria for the selection of resistant plants.
The objectives of this study were: (a) to analyse ontogenetic changes in the expression of morphological and biochemical components of resistance of sorghum to anthracnose, and (b) to establish the mode of inheritance of field resistance to the pathogen in adult plants.
MATERIALS AND METHODS
Plant materials and fungal cultures. Sorghum cultivars SC326-6 (IS3758 der, Nigricans) and SC599-11E (IS17459 der, Nigricans-Feterita), which are resistant (R) to C. graminicola, and B35-6 (IS12555 der, Durra) and BTx623 (BTx3197 [Combine Kafir60B] * SC170-6 [IS12661 der, Zerazera]), which are susceptible (S) to C. graminicola, were used for this study. These cultivars were chosen for their similar maturity, and R x S crosses were made to generate F1, F2, and F2-derived F3 progenies. The resistant commercial hybrid DK18 (DEKALB Genetic, Corp., Dekalb, Illinois) which has been well characterised for its phytoalexin response (Hipskind et al., 1990) was used as a standard in part of the study.
Isolates Cg13.89 and Cg20.89 (Texas) and Cg53.89 (Georgia) of C. graminicola were obtained from diseased plants collected in the field. The isolates were grown on oatmeal agar (7.25 %, w:v) treated with ampicillin (0.1 %, v:v) and streptomycin (0.1 %, v:v) at 23 °C under constant fluorescent light (60 µE m-2 s-1) to limit mycelial growth and induce sporulation (Nicholson and Moraes, 1980; Yang et al., 1991). Two-week old plates were flooded with distilled water supplemented with the wetting agent Tween 20 (1 µl ml-1) and conidia were gently scrapped off the plates. Spore density was determined with a hemacytometer and adjustments were made to the desired inoculum concentration for the experiments.
Symptom expression. All four inbred lines were grown in standard organic soil mix supplemented with mineral fertilisation (Bacto potting soil) in the greenhouse at College Station, Texas, during the summer of 1991. Inoculation was done weekly, starting at one week after emergence, with conidial suspensions (106 conidia ml-1) of all three isolates of C. graminicola. Noninoculated plants that had been sprayed with the water-Tween 20 solution (1 µl ml-1) were used as controls. The plants were incubated in the dark at 100% relative humidity for 15 hours. Two replications of a completely randomised design were used and data were recorded on the time to symptom expression (latent period), reaction type, persistance of symptoms, and symptom severity.
Time to symptom expression was taken as the average number of days elapsed between inoculation and the appearance of symptoms. Reaction type was classified as incompatible (with two subclasses, hypersensitive or lesion delimitation) for a resistant phenotype or compatible for a susceptible phenotype. Distinction between these types followed the principles discussed by Johal and Rahe (1990) for the interaction of the common bean with C. lindemuthianum. Symptom persistence was measured as the number of days elapsed between symptom appearance and disappearance (recovery), if any. Symptom severity was assessed three weeks after inoculation on a visual scale of 1 (lesion absent) to 5 (coalescent lesions covering 100% of the inoculated leaf area or plants dead).
Biochemical characterisation of resistance. Resistance of plants to infection by mycopathogens that produce toxins is considered the same as resistance to the pathotoxin itself. By analogy, resistance as measured by morphological indicators could be equated with the ability of host antibiotics to restrict, inhibit, or kill invading pathogens (Wood et al., 1972). On this basis, we carried out a time-course analysis of the phytoalexin profile of parental lines and R x S F1 plants inoculated with the three isolates of C. graminicola. A split-plot within a completely randomised design was used with fungal isolates as main plot treatments and test lines as subplot treatments.
Seeds were imbibed for 6 hours in aerated water at 28 °C after which they were placed between layers of moist germination paper in small containers and grown in the dark at 28 °C for 96 hours. This provided uniform development of seedlings as well as uniform first internode elongation. Four-day-old seedlings were inoculated on the first internode surface and placed in an incubator at 100% relative humidity with an initial four-hour-photoperiod to stop elongation (Nicholson et al., 1987). This was followed by alternating cycles of 9 hours dark - 15 hours light for 72 hours. Approximately 2.5 mg of excised first-internode sections were collected at 12 hour-intervals and placed in Eppendorf microfuge tubes containing 500 µl of high performance liquid chromatography (HPLC) grade methanol.
The compounds were allowed to leach into the methanol overnight at 4°C. Each methanol extract was centrifuged (Brinkmann Eppendorf Model 5414, 16,000 g, 10 min), and the supernatant was analysed by HPLC following the procedure of Hipskind et al. (1990). Three replications were used and extracts of noninoculated plants that had been sprayed with the water-Tween 20 solution were used as controls.
Three phytoalexins were assessed: luteolinidin, apigeninidin, and a caffeic acid ester of arabinosyl 5-O-apigeninidin, with molecular weights of 271.3, 255.3, and 549.5, respectively (Hipskind et al., 1990). Phytoalexin content was expressed as µmol g-1 of fresh tissue.
Inheritance of field resistance. The inheritance of resistance to strain Cg20.89 of C. graminicola was determined from two series of replicated field experiments.The first series consisted of the families SC599-11E * B35-6 and SC599-11E * BTx623 and were conducted in 1991 and 1992 at a single location, the Texas A&M University research farm near College Station. For each family, both parents, the F1, and 50 F2-derived F3 progenies were grown.
In 1991, sowing was done on 28 March and plants were inoculated with a conidial suspension (105 spores ml-1) of the pathogen at the time of anthesis (26 May) and on 4 June, to ensure adequate infection levels. In 1992, the sowing date was 31 March and the first and second inoculation were done on 2 June and 14 June, respectively.
The second series consisted of parental, F1, and F2 individuals of the families SC326-6 * BTx623, SC326-6 * B35-6, SC599-11E * BTx623, and SC599-11E * B35-6 which were sown on 26 March 1992 at College Station. Inoculation was performed as described above.
For both series, the statistical design was a randomised complete block design with three replications. Plot size consisted of one row for the parents and the F1 progeny and three rows for the F2 individuals. Row length was 5 m, and spacing was 80 cm between rows and 20 cm within rows, both in 1991 and 1992.
Anthracnose response was determined one week and four weeks following the second inoculation and classified as resistant (hypersensitive reaction to no more than 10% leaf area infected as observed in the R parents) or susceptible (more than 10% leaf area infected and with sporulation).
Statistical analysis. Data on time to symptom expression, symptom severity, and phytoalexin content were subjected to analysis of variance and separation of means using the GLM procedure in SAS (SAS Institute, 1985). Field data were subjected to C2 analysis to test for Pearson's goodness-of-fit to specific genetic segregation ratios.
RESULTS AND DISCUSSION
Symptom expression. Symptoms were not detected on seven-day-old seedlings of the resistant line SC326-6 regardless of the isolate of C. graminicola used to inoculate plants. The other resistant line, SC599-11E, was also immune to isolates Cg13.89 and Cg53.89 in seven-day-old seedlings. However, SC599-11E seedlings succumbed to isolate Cg20.89 21 days after inoculation (Table 1). Symptoms were expressed in both juvenile and older seedlings of the susceptible lines BTx623 and B35-6 inoculated with the agressive isolates Cg13.89 and Cg20.89. Inoculation with the least aggressive isolate Cg53.89 did not cause symptoms in seedlings less than 3 weeks old for all lines (Table 1).
TABLE 1. Effect of plant age on average time to symptom expression in resistant and susceptible sorghum lines inoculated with virulent (Cg13.89, Cg20.89) and avirulent (Cg53.89)isolates of Colletotrichum graminicola
a: "-" indicates that no symptoms were observed up to 35 days after inoculation; ± indicate the standard errors of the means
Beyond seven days after emergence, time to symptom expression was essentially the same for all lines and appeared to be related to the aggressiveness of the isolate considered. For example, the resistant inbreds did not develop any symptoms when inoculated with Cg53.89 for up to four weeks of age compared to three weeks for the susceptible inbreds. In general, reaction caused by the aggressive isolates Cg13.89 and Cg20.89 was expressed in all four inbreds within seven days of inoculation (Table 1). Thus, older plants of resistant and susceptible lines did not differ in their initial response to infection. Rather, the data suggest that resistance may be associated with the speed at which the host is capable of preventing further spread from the area of initial infection.
Other characteristics of the resistant phenotype include type, spread, persistence, and severity of symptoms, all of which were reported to be plant-age dependent (Andersen et al., 1947). In this study, all lines initially expressed a highly localised lesion type regardless of plant age or source of inoculum. Some variation was found for the size of the area covered by lesions, which was attributed to differences in the amount of inoculum applied to leaf surfaces. Single lesions, presumably due to single conidia, were all very restricted (ca. 0.67 mm in diameter).
Subsequent symptom development varied with genotype and age at time of inoculation. In the resistant line SC326-6, only isolated necrotic flecks were detected. These did not enlarge with time and were considered typical of the hypersensitive response (Johal and Rahe, 1990). In SC599-11E, expansion of the necrotic area was not prevented. Instead, the size of the lesions increased over 3-4 days to cover approximately 10-30 % of leaf area and, then, lesion expansion was prevented. This was classified as a lesion delimitation type of resistance (Johal and Rahe, 1990).
While susceptible lines also initially responded with a hypersensitive reaction, they were unable to restrict pathogen growth, since lesion expansion proceeded to produce large, coalescent necrotic and chlorotic tissues, hence their relatively high severity scores. This was particularly true of older plants (Fig. 1).
Figure 1. Time to symptom expression (days) as affected by plant age in resistant (SC326-6,SC599-11 E) and susceptible (BTx623, B35-6) sorghum lines responding to inoculation with virulent (Cg13.89, Cg20.89) and avirulent (Cg53.89) isolates of Colletotrichum graminicola. Arrows indicate that no symptoms were observed.
Regardless of symptom type, all lines expressed signs of recovery from infection when they were inoculated prior to three weeks of age, but not beyond that stage. Although the biological basis for this phenomenon was not investigated, these data suggest that resistance assessment based solely on juvenile plants may not be indicative of the adult plant response. In this regard, the present study differs from the work of Ferreira and Warren (1982) who found a positive and significant correlation (r=0.87**) between the disease severity index of 35-day-old and 52- or 62-day-old plants of 23 sorghum lines.
Biochemical characteristics of resistance. Data obtained with the hypersensitive resistant line (SC326-6) and the most susceptible line (BTx623) indicate that the most fungitoxic phytoalexin, luteolinidin (Hipskind et al., 1990), accumulated to greater levels in the resistant than in the susceptible line (Fig. 2). Furthermore, this compound began to appear in the resistant line as early as 12 and 24 hours post-inoculation in response to attempted ingress by aggressive isolates Cg20.89 and Cg13.89, respectively, compared to 48 hours for the susceptible line challenged with either isolate.
Figure 2: Ontogenic effects on the anthracnose response of genetically resistant (SC326-6 and SC599-11E) and susceptible (BTx623 and B35-6) sorghum lines innoculated with virulent isolates Cg13.89 (a) and Cg20.89 (b) and avirulent isolate Cg53.89 (c) of Colletotrichum graminicola.
Apigeninidin displayed the highest rate of accumulation in the first 24 hours following inoculation in both compatible and incompatible interactions of sorghum lines with C. graminicola isolates. As a result, the content of apigeninidin was the highest of the three phytoalexins until 36 hours after inoculation with the non aggressive isolate and 48 hours after inoculation with the aggressive isolates (Fig. 3).
Figure 3: Time course production of apigeninidin (APG), luteolindin (LUT) and an acyl ester derivative of apigenindin (CAE) by a resistant line, SC326-6 (SC) and a susceptible line BTx623 (BT) of a sorghum innoculated with virulent (Cg13.89, Cg2089) and avirulent (Cg53.89) isolates of Colletotrichum graminicola.
Although detection of the other two compounds lagged behind that of apigeninidin, luteolinidin content increased over time as did the content of the caffeic acid ester in both sorghum lines responding to the aggressive isolates of C. graminicola. Luteolinidin became the major phytoalexin in the resistant line, 60 hours following inoculation. This contrasted with the reaction of the susceptible line in which the caffeic acid ester became the predominant compound after 60 hours and 72 hours of interaction with Cg20.89 and Cg13.89, respectively. Interaction of either sorghum line with the non aggressive isolate Cg53.89 also resulted in higher accumulation of the caffeic acid ester 48 hours following inoculation despite initial preponderance of the other phytoalexins (Fig. 3).
Hipskind et al. (1990) showed that luteolinidin was the most inhibitory compound of the sorghum phytoalexins, followed by apigeninidin and the caffeic acid ester. Because luteolinidin differs from apigeninidin by a single hydroxyl group, it is possible that apigeninidin is the first compound to be synthesised. This would be consistent with its earlier detection and greater prevalence in early hours of the interaction between sorghum lines and C. graminicola isolates. Excess apigeninidin could similarly be converted to the caffeic acid ester, which is the least fungitoxic of the compounds. Also consistent with our hypothesis on the biochemical relationships and relative efficiencies of the sorghum phytoalexins was the greater accumulation of the caffeic acid ester in the susceptible sorghum lines than in the resistant lines when exposed to virulent isolates whereas the opposite was observed for luteolinidin content. This suggests that resistance in SC326-6 could reside in its higher efficiency at converting apigeninidin into luteolinidin, whereas susceptibility of BTx623 could be attributed to a lower efficiency, thus the accumulation of the least fungitoxic compound in the susceptible line. No difference was found between the response kinetics of the resistant line and the susceptible line when exposed to the non aggressive isolate Cg53.89, except that phytoalexin production was higher in the resistant line.
The response pattern of the susceptible line B35-6 was essentially the same as for BTx623. However, the response profiles of resistant lines were similar when exposed to isolates Cg13.89 and Cg53.89 but different when exposed to isolate Cg20.89 to which SC599-11E succumbed after an initial resistant reaction.
Inheritance of field resistance. Cultivar SC326-6 displayed a hypersensitive resistance to the isolate assayed, regardless of growth stage. In contrast, SC599-11E was initially resistant but failed to restrict fungal colonisation as the plant aged, which resulted in complete reversal of its phenotype. These response patterns of the resistant sources were conserved in their progeny (Table 2).
TABLE 2. Anthracnose response of inbred and F1 lines of sorghum inoculated with Isolate Cg20.89 of Colletotrichum graminicola at College Station, Texas, during 1992 growing season
: R= number of resistant plants, S= number of susceptible plants. Plants were classified as resistant when they displayed a hypersensitive reaction or had no more than 10% leaf area infected (as observed in the R parents). They were considered susceptible otherwise (more than 10% leaf area infected and with sporulation)
TABLE 3. Segregation and C2 analysis of resistance to isolate Cg20.89 of Colleotrichum graminicola in sorghum families evaluated at CollegeStation, Texas, during 1991 and 1992growing seasons
a: R= number of resistant plants, S= number of susceptible plants
The F1 progenies of the crosses SC326-6 * BTx623 and SC326-6 * B35-6 were phenotypically the same as SC326-6 regardless of the developmental stage of the plants, suggesting complete dominance of resistance from SC326-6. Pearson's goodness-of-fit test for a 3:1 segregation in the F2 generation produced C2 values of 0.052 and 0.103 for the cross SC326-6 * BTx623 at one and four weeks following inoculation, respectively. The corresponding statistics for the cross SC326-6 * B35-6 were 0.355 and 2.094 (Table 3). None of these C2 values was significant at 0.05 probability level, thereby suggesting a condition of single dominant gene inheritance of anthracnose resistance from line SC326-6.
When SC599-11E was crossed to either BTx623 or B35-6, the F1 progeny was resistant one week following inoculation. The goodness-of-fit test for a segregation of 3 resistant: 1 susceptible produced nonsignificant (P < 0.05) C2 values of 1.786 for SC599-11E * BTx623, and 0.117 for SC599-11E * B35-6 (Table 3). When anthracnose response was evaluated four weeks after inoculation, no resistant plant was found in the F1 or F2 generation.
Interestingly, single gene segregation followed by loss of resistance was found in the F2:3 families of the crosses SC599-11E * BTx623 and SC599-11E * B35-6 both in 1991 and 1992. Ontogenic changes in phenotypic expression could not be investigated beyond the F2 generation for the crosses SC326-6 * BTx623 and SC326-6 * B35-6 due to the lack of seed.
Nevertheless, field results confirmed our findings from greenhouse studies that the genetic basis for anthracnose resistance in SC599-11E is not the same as in SC326-6. Barring the very unlikely possibility that ontogenic changes in symptom expression of SC599-11E - derived families merely reflected leaf senescence (Nicholson et al., 1985), the present study suggests multiallelism at a single locus as the genetic basis for anthracnose resistance in sorghum. It is proposed that this locus be referred to as "Cgl" for resistance to the leaf disease phase of anthracnose. This symbol emphasises more the causal organism of anthrachnose, C. graminicola, than did previously suggested symbols "l" (LeBeau and Coleman, 1950) or "ls" (Coleman and Stokes, 1954).
Under the multiple allelle hypothesis, the allele responsible for resistance in SC599-11E (cglr) would be recessive to the allele conferring resistance to SC326-6 (Cgl) but dominant to the allele present in the susceptible lines (cgl ). Additionally, the SC326-6 allele would provide durable protection against the invading fungus unlike the allele in SC599-11E.
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