CSIRO PUBLISHING
Australasian Plant Pathology, 2009, 38, 632–637
www.publish.csiro.au/journals/app
Effect of temperature and relative humidity on sorghum ergot development in northern Mexico N. Montes-García A,D, L. K. Prom B, H. Williams-Alanis A and T. Isakeit C A
National Institute for Forestry, Agriculture and Livestock Research (INIFAP), Rio Bravo Experimental Station (CERIB), A. P. 172, Rio Bravo, Tamaulipas, CP 88900, Mexico. B United States Department of Agriculture-Agricultural Research Service (USDA-ARS), 2765 F&B Road, College Station, Texas 77845, USA. C 2132 Texas A&M University, College Station, Texas 77845, USA. D Corresponding author. Email:
[email protected]
Abstract. Trials were planted at Rio Bravo, Tamaulipas, Mexico, during 2002 and 2003 with the objective of determining the relationship between sorghum ergot severity and weather factors, and to develop a risk assessment model. Six sorghum hybrids and three male-sterile genotypes were planted every month from January to October. At anthesis initiation, inoculation was conducted using a local isolate of Claviceps africana. Among hybrids, there was a negative relationship between ergot severity and maximum and minimum temperatures, with the highest significant correlation of –0.71 from 7 to 9 days before anthesis. During this period, minimum temperatures above 10C increased the risk of ergot development, whereas minimum temperatures above 22.5C prevented ergot development. In male-sterile plants, ergot was negatively related to maximum temperature after anthesis, with ergot being observed at maximum temperatures up to 38C. Minimum relative humidity showed a positive and significant correlation with ergot severity. Values of minimum relative humidity above 30% during anthesis promoted infection. Surface response regression models were developed for the effects of minimum relative humidity and minimum and maximum temperature during the infection process on ergot severity.
Introduction The worldwide appearance of sorghum ergot, caused by Claviceps africana, poses a serious threat to sorghum seed production fields and commercial grain fields (Aguirre et al. 1997; Isakeit et al. 1998; Wang et al. 2000). The pathogen mainly infects stigmas, and occasionally ovaries, but ultimately invades unfertilised ovaries (Futrell and Webster 1965; Bandyopadhyay et al. 1998). Male-sterile lines used in hybrid seed production fields are the most vulnerable to ergot infection, especially when environmental factors reduce pollen quality and viability (Futrell and Webster 1965; Bandyopadhyay et al. 1998). In northern Mexico, where the pathogen is endemic, losses up to 100% in seed production fields and 30–35% losses in sorghum commercial fields have been observed. Losses in commercial fields have been attributed to hybrid pollen sterility due to exposure to low temperatures when they are planted in mid September to early January. To reduce the impact of this disease in the area, a crop management strategy is needed. Critical skills for disease management are early diagnosis, knowledge of the behaviour of the pathogen in a specific geographic area, and the ability to forecast disease development. Weather conditions that influence epidemics play an important role for ergot outbreaks (Wang et al. 2003) by their direct effects on the pathogen and pollen production (McLaren and Flett 1998) in sorghum hybrids and restorer lines, and in the pollination and fertilisation processes in seed production Australasian Plant Pathology Society 2009
fields (Bandyopadhyay et al. 1996). C. africana readily infects florets of male-sterile plants in the absence of viable pollen. Therefore, florets of self-fertile plants may become infected due to sterility induced by certain environmental conditions. Any factor that increases the period between floret opening and fertilisation will promote ergot infection (Futrell and Webster 1965). Downes and Marshall (1971) demonstrated that night temperatures of 13C or lower during meiosis could induce sorghum pollen sterility in some genotypes. Meanwhile, Brooking (1976) observed that once ovaries are fertilised, they develop normally even during cool weather. Also, he found that the period of cold temperature sensitivity of a sorghum panicle extends from the emergence of the flag leaf ligule to the time when the flag leaf is 20 cm in length. Temperatures of 10–12C are required for several days to induce complete sterility of the sorghum panicle. If there is a short interruption of such temperatures, only some portions of the panicle may be affected. The relationship between the sterility induced by cold temperatures and ergot susceptibility was demonstrated by McLaren and Wehner (1992), who observed that some sorghum genotypes grown at 12C for 3–4 weeks before anthesis were susceptible to ergot. In recent studies, Montes et al. (2003b) observed a significant effect between the minimum temperatures below 13C and ergot incidence in sorghum hybrids, especially if these temperatures were present between 9 and 11 days before anthesis (around boot stage). Similarly, Wang et al. (2003) assumed male sterility in 10.1071/AP09049
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Sorghum ergot and weather factors
Materials and methods Trials were planted in 2002 and 2003 at Rio Bravo (RB), Tamaulipas (northern) Mexico (25580 N, 98000 W), which has a mean annual precipitation of 500 mm with a mean annual temperature of 23.1C. It was chosen because it is located in one of the largest sorghum grain production and seed production areas of Mexico. Sorghum hybrids AP 2233 (Syngenta, Wilmington, DE, USA), KS 310 (Sorghum Partners, New Deal, TX, USA),
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NC+ 7W97 (NC+ seeds, Lincoln, NE, USA), GARST 5664 (Syngenta), ATx399 Tx430 (Texas A&M University, College Station, TX, USA), NC+8R18 (NC+ seeds) and male sterile A-lines ATx635, ATx2752 and ATx623 (all Texas A&M University, College Station, TX, USA) were planted every month from January to October. Hybrids were chosen based on previous ergot reaction studies conducted during the period from June to December in Weslaco, Texas (Isakeit et al. 1999), and similarities in flowering pattern. Plants were grown in a complete randomised block design with four replications. At every sowing date, each entry was planted in a single 5-m-long row, with a row spacing of 80 cm, resulting in a population of ~125 000 plants/ha. Weeds were controlled by hand hooded sprayer with Roundup (Monsanto, St Louis, MI, USA) at 25 mL/ha per 12 L of water. Sorghum midge (Contarinia sorghicola) was controlled as needed with Asana XL (Dupont, Wilmington, DE, USA) (70 mL/ha). The trials were furrowirrigated at least twice after planting, with the first irrigation at 45 days after planting (DAP) and the second one at 75 DAP. In each row, five panicles of similar maturity were selected and tagged (total genotype sample = 20) at appearance of the first stigmas in the upper part of the panicle. Inoculation was conducted using a local C. africana isolate. Inoculum was increased on male-sterile line ATx623 under greenhouse conditions. Targeted panicles were marked and inoculated twice (every second morning) between 8.00 a.m. and 10.00 a.m. using a hand atomiser until runoff with a suspension of 1.6 106 conidia/mL from anthesis initiation until full bloom of each plant. Ergot severity (percentage of infected florets observed at each inoculation date) was measured at milk stage (10–12 days after initiation of anthesis). The percentages of infected florets were estimated visually. The individual ergot severity values for the 20 panicles were averaged separately for the hybrids and A-lines, so that individual points on Figs 1–5 represent pooled values for the hybrids or A-lines at each planting date. The period from initial and final anthesis dates for each inoculated panicle were recorded (the period varied depending on weather conditions and type of plant i.e. A-lines showed a wider period than hybrids).
100 Y = 82.02308 + 2.19015X – 0.11818X 2 R 2 = 0.67
90
Ergot severity %
sorghum grain hybrids if the mean daily minimum temperature during flag leaf stage was less than 13C. The ideal weather conditions for sorghum ergot development are temperatures around 19C, high relative humidity (RH), and cloudy conditions during anthesis (McLaren and Wehner 1990; Workneh and Rush 2002). Ergot is reduced with increasing temperature and it does not occur at maximum temperatures exceeding 28–30C (McLaren and Wehner 1990; Workneh and Rush 2006). Gupta et al. (1983) observed that C. microcephala (cause of pearl millet ergot) was not observed at air temperatures exceeding 32C. The optimum RH for disease development is closer to 100% during the infection process (Futrell and Webster 1966). Workneh and Rush (2002) observed that prevalence of ergot was related to the average RH and precipitation. These same authors suggested that minimum temperature is less of a factor than maximum temperature in development of sorghum ergot in the Texas Panhandle seed production area. They observed measurable infection occurred at a maximum temperature of 34C with a spore concentration of 106 spores/mL whereas there was no infection at 30C with a 104 spores/mL spore concentration, indicating that the infection rate depends on an interaction between temperature and amount of inoculum. High humidity can delay anther dehiscence and release of pollen (Quinby 1958). However, Ryley (2005) found that the time of maximum pollen release for at least one sorghum hybrid was in the early morning when RH was >90%. He found that rainfall during this period significantly reduced the release of pollen. Weather parameters also influence the biology of the pathogen. Temperatures between 14 and 28C, combined with high RH (>90%), are required for secondary conidiation and for conidial dispersion, but they are not required for sphaceliumsclerotium differentiation (Bandyopadhyay et al. 1996). The effect of temperature on secondary conidia germination were observed by Bhuiyan et al. (2002), who showed that secondary conidia germinated up to 37C, although the optimum was 20C. Generally, a disease model is developed to estimate the probability or risk of an undesirable event occurring at a given location and time (De Wolf et al. 2003). The reason for developing models is because growers need decision systems for plant disease management. Usually, models involve the interaction among factors described by Vanderplank (1963) in the disease triangle such as pathogen, environment and host. The objective of this study was to understand the relationship between sorghum ergot and weather factors and to develop a risk assessment model for northern Mexico, to advise growers, seed companies and scientists about the ergot risk on different sorghum genotypes.
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80 70 60 50 40 30 20 10 0
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Maximum temperature °C Fig. 1. Effect of maximum temperature recorded 4–6 days after anthesis initiation on ergot severity observed in sorghum A-lines.
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Y = –6.39216 + 18.11127X – 1.51920X 2 + 0.03227X 3 R 2= 0.63
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90 Y = 48.65453 + 4.82903X – 0.26141X 2 R 2= 0.45
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80 70 60 50 40 30 20 10 0 0
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Minimum temperature °C Fig. 3. Effect of minimum temperature recorded 1–3 days after anthesis initiation on ergot severity observed in A-lines.
100 90
Y = 27.696 – 1.50207X + 0.02057X 2 R 2= 0.65
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Minimum temperature °C Fig. 2. Effect of minimum temperature recorded 7–9 days before anthesis initiation on ergot severity observed in sorghum hybrids.
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Fig. 5. Predicted effect of minimum relative humidity (1–3 days after anthesis initiation) and maximum temperature (4–6 days after anthesis initiation) on ergot severity in A-lines in northern Mexico.
sorghum plants, these weather parameters were measured during the 2002 and 2003 growing seasons. Weather triad values, consisting of the mean of 3 consecutive days (e.g. mean of the maximum temperature recorded on each of the 3 days) were obtained (e.g. daily maximum and minimum temperatures and minimum RH; HRMIN) from the National Institute for Forestry, Agriculture and Livestock Research weather station located near the experimental site. Since RB had high (~100%) maximum RH during the whole year, RHMIN was used. Disease severity was transformed using the arcsine of the square root of ergot severity to satisfy assumptions of normality. To obtain each triad value, a 30-day period before anthesis for each panicle was used. This period was divided into 10 stages, each consisting of 3 days. Also, a period up to 9 days after anthesis was considered in the analysis and divided into three stages. Data values were pooled over both years and Pearson’s correlation coefficient (PROC CORR; SAS Institute, Cary, NC) was performed to identify the stages when there were the highest correlations between ergot severity and weather parameters. Polynomial models derived from multiple regression (PROC REG; SAS Institute) analysis were chosen based on the highest coefficient of determination and the lowest mean square error value. Data were used to generate surface response regression models capable of predicting ergot severity.
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Minimum relative humidity % Fig. 4. Effect of minimum relative humidity recorded 1–3 days after anthesis initiation on ergot severity observed in sorghum hybrids.
Since previous studies (McLaren and Flett 1998; MontesBelmont et al. 2002; Montes et al. 2003a; Workneh and Rush 2006) suggested that weather factors such as maximum temperature (TMAX), minimum temperature (TMIN), and RH are the most important determinants of ergot susceptibility in
The results of the correlation coefficient analyses are given for hybrids and A-lines. The polynomial models are then discussed. For hybrids, there was a negative relationship between ergot severity and TMAX, with the highest significant correlation coefficient of –0.71 at boot stage (7–9 days before anthesis initiation) (Table 1). Ergot severity was also negatively related to TMAX values in post-flowering stages. Similar results were observed with A-lines. They had a highly significant correlation of –0.71 between ergot severity and TMAX from 4 to 6 days after anthesis initiation. There was a highly significant correlation between ergot and TMIN during the pre-flowering stages of sorghum hybrids (Table 1). A negative relationship was found, especially from
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Table 1. Pearson’s correlation coefficientsA between ergot severity and weather variables observed in sorghum genotypes evaluated at Rio Bravo, Mexico TMAX, maximum temperature; TMIN, minimum temperature, HRMIN, minimum relative humidity Period
Hybrids TMIN
TMAX
HRMIN
A-lines TMIN
TMAX
HRMIN
28–30 25–27 22–24 19–21 16–18 13–15 10–12 7–9 4–6 1–3
–0.55 –0.54 –0.55 –0.57 –0.58 –0.60 –0.70 –0.71 –0.66 –0.66
** ** ** ** ** ** ** ** ** **
–0.54 –0.48 –0.48 –0.53 –0.58 –0.63 –0.69 –0.69 –0.59 –0.68
** ** ** ** ** ** ** ** ** **
Days before anthesis initiation 0.19 * 0.29 ** 0.28 ** 0.41 ** 0.31 ** –0.01 n.s. –0.06 n.s. –0.03 n.s. 0.07 n.s. 0.14 *
–0.23 –0.26 –0.32 –0.36 –0.46 –0.56 –0.59 –0.59 –0.62 –0.68
** ** ** ** ** ** ** ** ** **
–0.29 –0.34 –0.18 –0.33 –0.47 –0.46 –0.54 –0.57 –0.56 –0.59
** ** ** ** ** ** ** ** ** **
0.04 0.13 0.22 0.01 0.04 0.08 0.22 0.26 0.36 0.38
n.s. n.s. ** n.s. n.s. n.s. ** ** ** **
1–3 4–6 7–9
–0.65 –0.68 –0.64
** ** **
–0.65 –0.64 –0.68
** ** **
Days after anthesis initiation 0.56 ** 0.09 n.s. –0.06 n.s.
–0.71 –0.65 –0.63
** ** **
–0.61 –0.59 –0.57
** ** **
0.55 0.49 0.52
** ** **
A
Correlation coefficients were obtained using 2400 (hybrids) and 1200 (A-lines) data values for each weather variable. ** = statistically significant at P < 0.01; * = statistically significant at P < 0.05; n.s. = not significant.
7 to 12 days before anthesis initiation. Results were similar with the A-line plants in which there was a high negative correlation 1–3 days after anthesis initiation. The correlation coefficient between RHMIN and ergot severity in hybrids was positive and significant, especially at 1–3 days after anthesis initiation (r = 0.56) (Table 1). Also A-lines showed a highly significant correlation (r = 0.56) between ergot severity and RHMIN during the same period (Table 1). A polynomial regression of observed ergot severity data on A-lines against TMAX 4–6 days after anthesis initiation (Fig. 1), showed that the ideal weather conditions for maximum ergot expression were maximum temperatures around 23C, while ergot did not develop at maximum temperatures of 38C. According to the polynomial models TMIN during 7–9 days before anthesis initiation had a significant effect on ergot severity in sorghum hybrids (Fig. 2), in which cooler minimum temperatures around 10C increased ergot severity. Ergot severity was low when TMIN was above 22.5C during 7–9 days before anthesis initiation. A-line plants also showed a highly negative relationship between ergot and TMIN recorded at 1–3 days after anthesis initiation. The relationship of TMIN to ergot is shown in Fig. 3, which shows higher disease at lower TMIN (below 20C). Also, the polynomial model shows that ergot is diminished with TMIN greater than 25C during this period. A-lines showed a highly significant correlation between ergot and RHMIN during the anthesis period (Table 1). The effect of RHMIN on ergot in hybrids is shown in Fig. 4. The polynomial regression model suggests that values above 40% RHMIN are needed to support ergot presence. Weather data that had a relationship to ergot were subjected to a two-factor surface response regression model. The resulting
prediction models were statistically significant for hybrids and A-lines. A-lines were affected by TMAX, where they promoted ergot development with increasing RHMIN around anthesis. The obtained surface regression model was: Y ¼325:82þ16:73ðTMAXÞþ3:69ðHRMINÞ0:29ðTMAXÞ2 0:01ðTMAXHRMINÞ0:02ðHRMINÞ2
ð1Þ
where Y = ergot percentage severity; TMAX = mean maximum temperature from 4 to 6 days after anthesis initiation; and HRMIN = mean minimum relative humidity from 1 to 3 days after anthesis initiation. This model accounted for more than 60% of the total variation of the observed data and was highly significant (Fig. 5). The predicted ergot infection was very high, especially when high values of RHMIN and TMAX were combined. Maximum ergot severity was around 30C with RHMIN near 100%. The ergot prediction model for sorghum hybrids was also affected by the combination of RHMIN and TMIN, especially minimum temperatures during 7–9 days before anthesis initiation, and RH during anthesis. The model obtained was: Y ¼ 117:95 þ7:39ðTMINÞ þ 3:23ðHRMINÞ 0:16ðTMINÞ2 0:09ðTMIN HRMINÞ 0:01ðHRMINÞ2
ð2Þ
where Y = ergot percentage severity; TMIN = mean minimum temperature from 7 to 9 days before anthesis initiation; and HRMIN = mean minimum relative humidity from 1 to 3 days after anthesis initiation. According to the model, ergot would develop under humid conditions if there was a decrease in the temperature at 7–9 days before anthesis. The model accounted for 50% of the variation of the data (Fig. 6).
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0 30
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Temperature Fig. 6. Predicted effect of minimum relative humidity (1–3 days after anthesis initiation) and minimum temperature (7–9 days before anthesis initiation) on ergot development in sorghum hybrids in northern Mexico.
Discussion The main objective of this study was to determine the relationship between ergot severity and weather variables in Mexico, which was obtained and reflected in ergot potential models. The results and the models derived from the present study assume the presence of viable and abundant C. africana inoculum. Since sorghum ergot is a disease that can be prevented by rapid fertilisation of the ovary, we inoculated the same panicle every second day because we wanted to have a high disease pressure to observe the tolerance or resistance of the genotypes throughout the anthesis period. We observed that sorghum ergot caused by C. africana was influenced by weather factors. These results are similar to those obtained by Gupta et al. (1983), who observed that rainfall, sunshine hours, RH and air temperature accounted for almost 100% of the variation in ergot. In this study, as in others (McLaren and Wehner 1990; McLaren and Flett 1998; Wang et al. 2000, 2003; Montes et al. 2003a, 2003b; Workneh and Rush 2006), favourable weather conditions before and after anthesis promoted sorghum infection by C. africana. However, high temperature and low RH inhibited the disease. Ergot development was very sensitive to a moist environment. These results suggest that high humidity provided by rain or morning and afternoon drizzle promotes infection. Male-sterile plants showed that the ideal weather conditions for maximum sorghum ergot expression are maximum daily temperatures around 23C. However, this study suggests that ergot can develop when maximum daily temperatures are up to 38C. This is consistent with results obtained by Bhuiyan et al. (2002), who showed that ergot conidia germinated up to 37C, whereas temperatures above this inhibited the infection by C. africana. This may be due to the inhibition of germ tube growth above this temperature, as shown for C. microcephala (Gupta et al. 1983). These results differ from those of McLaren and Wehner (1990) and Workneh and Rush (2006), who observed that the ideal temperature for sorghum ergot development is around 19C, and that ergot is reduced with increases in temperature, until it is stopped at temperatures exceeding 30C. This difference may be because we inoculated the same panicle at least twice with a high amount of inoculum to create a
high disease pressure. Nevertheless we detected the same results as Workneh and Rush (2002), who observed that ergot infection rate increased as inoculum and temperature increased. Our results indicate that the C. africana isolate present in our area may be adapted to more tropical conditions and can be more pathogenic under warmer conditions such as northern Mexico and south Texas, USA. The high correlation between ergot severity, TMIN, TMAX and RHMIN in this study, as well as results from the studies of McLaren and Wehner (1990), McLaren and Flett (1998) and Montes et al. (2003a) reaffirms the close relationship between weather variables and ergot severity in sorghum. In general, weather factors that had a high correlation with ergot severity, showed the highest correlation coefficients around anthesis. Nevertheless, with hybrids, TMAX and TMIN values before initiation of anthesis had a direct effect on ergot, especially those present 7–9 days before anthesis initiation. This represents a high risk for ergot, because low night temperatures before anthesis (Brooking 1976; McLaren and Wehner 1992; Montes-Belmont et al. 2002), or during pollen mother cell meiosis (Downes and Marshall 1971) and in the period between flag leaf ligule emergence and flag leaf sheath elongation (Brooking 1976; Wang et al. 2000, 2003) results in poor seed set due to nonviable pollen. Thus, male-sterility caused by low temperatures becomes a significant factor in the epidemiology of the disease. Ergot severity also showed a good relationship with TMAX values recorded after anthesis. Low temperatures after anthesis might also affect pollen release and secondary sporulation. Meanwhile, A-lines showed the greatest correlation with TMAX, TMIN and RHMIN coefficients after anthesis initiation. The differences in the response of ergot severity to weather between hybrids and male-sterile A-lines could be due to the genetic background of the A-lines, to their flowering pattern, and interference with infection because of pollination. Moisture is a key factor in the infection process of fungal pathogens. The results showed that RHMIN values from 40% present during the anthesis period were enough to promote ergot infection. This is quite similar to the results of McLaren and Wehner (1990), who found the period from 1 to 4 days after pollen shed to have the most significant relationship between ergot and RHMIN. It is clear that the hybrid seed production system in northern Mexico is at high risk because ergot can develop on A-lines during the normal growing season from February to August. Ergot infection during the winter season from October to January did not occur due to frost that reduced flower development and cooler temperatures that inhibited the pathogen. Models developed in this study consider the effect of weather factors during the infection process as well as plant predisposition (on hybrids). Ergot severity, assuming the presence of viable inoculum, can be accurately predicted. The predicted ergot potentials can be used as a tool in sorghum fields to: (1) distinguish the seed production risk, and (2) apply fungicides more efficiently, or (3) identify the possible crop windows where grain sorghum could be established and cultivated. The recommendation to farmers will be to plant sorghum hybrids in periods in which plants can avoid exposure to low minimum temperatures before flowering. For seed production fields, the recommendation will be to apply
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control measures (chemical control and crop management) to reduce ergot. The analysis of historical weather data and application of these models can give a better idea of the possible C. africana impact in sorghum hybrids and malesterile lines. Acknowledgements We thank William L. Rooney (Texas A&M University) for providing some of the genetic material used in this study. We also want to express our gratitude to Lauro Macias, Francisco Garcia, Ciro Longoria and Daniel Alvarado for their technical assistance during the course of this study. This research was developed between INIFAP and USDA-ARS, and was funded in part by the USDA/FAS/ICD/RSED grants 58–3148–7-026 and 586202–1-F151 to develop research on sorghum ergot.
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Manuscript received 25 November 2007, accepted 30 July 2009
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