valuable sources of resistance to stripe rust in synthetic hexaploid wheat

1
INTRODUCTION Puccinia. graminis f.sp. tritici is one of the debilitating wheat diseases worldwide. For at least two decades, stem rust of wheat was considered to be a disease of minor importance mainly due to the incorporation of Sr31 resistance gene in many of the bread wheat cultivars; however, this gene succumbed to a new stem rust race called Ug99 (TTKSK) (Pretorius et al., 2000). In Ethiopia, two types of wheat (hexaploid, Triticum aestivum L., and tetraploid, T. turgidum L) are cultivated under rain-fed conditions mainly by resource-poor farmers. Durum wheat (T.turgidum subsp. durum Desf.) is the predominating tetraploid, which is an indigenous crop in Ethiopia whereas bread wheat is an introduction, and most of the high yielding semi-dwarf bread wheat varieties are susceptible to Ug99 and other races prevalent in the country. In the absence of resistance in cultivated varieties, new sources of resistance are sought from landraces and related species. Ethiopia is endowed with an immense genetic diversity for tetraploid wheat. All the six species of wheat observed by Vavilov in the mid-1920s are still grown by farmers as landraces (IBC, 2007). The Ethiopian tetraploid landraces have been identified to be potential sources of disease resistance including stripe and stem rust (Betesellassie et al., 2007; Haile et al., 2012). The high level of diversity in these landraces allows breeders and pathologists to make selection for different traits of economic importance. Therefore, the major objective of this study was to identify sources of resistance in the Ethiopian durum wheat landraces to Ug99 and other prevailing races of stem rust at Debre Zeit, Ethiopia. MATERIALS and METHODS A total of 991 durum wheat landraces collected from different areas of Ethiopia (Tigray, Gondar, Gojjam, Wollo, Shewa and Kaffa) were used in this study. The collections were made and maintained as single lines by various researchers of durum wheat improvement program of Debre Zeit Agricultural Research Center. The experiment was conducted in 2009 and 2010 seasons. In 2009 main season, a total of 991 entries were tested whereas in 2010 off-season, 132 landraces selected from the main season were used. Each entry was planted in two rows of 1m length together with four checks (PBW343, Morocco, Ude and Yerer). PBW343 is carrying Sr31 gene (Brama et al., 2003), Morocco (susceptible check), Ude and Yerer are CIMMYT originated commercail durum wheat varieties in Ethiopia. The nursery was bounded by spreader rows planted with mixtures of susceptible durum (Arendeto and local red) and bread wheat (PBW343) varieties. The spreader rows were inoculated three times starting from stem elongation with mixtures of TTKSK (Ug99) and other races carrying virulences for stem rust resistance genes including Sr13 using the injection method (Roelfs et al., 1992). The rust assessment was made three times using the Modified Cobb’s scale (Peterson et al., 1948). The terminal severity was used to categorize the entries into resistant and susceptible groups. The severity was converted to coefficient of infection (CI) values by multiplying the severity by constant values (Roelfs et al., 1992). The constant values are: R= 0.2, MR=0.4, MS=0.8 and S=1. Based on the CI values, the entries were categorized under four resistant groups: The first group included the landraces with 0-10% severity (resistant), the second with severity 15-20% (moderately resistant), and the third with severity of 25-30% moderately susceptible whereas the rest were considered as susceptible. However, only entries which combined leaf and stem rust resistances were advanced to the next stage of evaluation in 2010 off-season. Worku Denbel 1* and Ayele Badebo 2 1 Ethiopian Institute of Agricultural Research (EIAR), Kulumsa Agricultural Research Center, P.O. Box. 489, Asella, Ethiopia 2 Debre Zeit Agricultural Research Center, P.O.Box 32, Debre Zeit, Ethiopia *Corresponding author: [email protected] RESULTS and DISCUSSION In 2009 main season, the leaf rust diseases pressure was quite high, and out of the total entries tested, only 4.8% were resistant, 13.2% were moderately resistant, 32.9% were moderately susceptible and the remaining 49.1% were completely susceptible to the disease (Figure 1). Leaf rust has been reported to be the most common disease wherever durum landraces are grown (Huluka and Andnew, 1992). In this study, almost all of the durum wheat landraces exhibited susceptible or moderately susceptible reaction to leaf rust; however, they varied in terminal severities. The absence of complete resistance to leaf rust in the landraces is also in agreement with the previous reports (Andenow et al., 1997; Huluka and Andenow, 1992). In Ethiopia, durum wheat and stem rust have co-evolved for thousands of years and this close association has resulted in the accumulation of a wider virulence spectrum on the side of the rust (Bechere et al., 1995). The use of durum wheat parents with low level of moderately susceptible or moderately resistant infection types is a valuable and a recommended breeding strategy which has been utilized for durum wheat improvement in Ethiopia (Bechere et al., 1995) and as a result of such breeding methodology a number of durum wheat varieties have been released by Debre Zeit Agricultural Research Center. In 2009 main season, stem rust incidence was relatively low and the highest stem rust severity was 50% on susceptible varieties. Out of 991 landraces evaluated for stem rust resistance, 79.5% exhibited resistance reaction, 10.6% were moderately resistant, 8% were moderately susceptible and the remaining 1.9% was completely susceptible (Figure 2). The low level of stem rust infection was attributed to the susceptibility of many of the landraces to leaf rust which appeared early in the season. Under such circumstances, it was difficult to select for stem rust resistance under field conditions since the tissue was being killed by leaf rust at early stages. Therefore, only 132 entries which combine stem and leaf rust resistances have been selected for the subsequent test. No. Entries Stem rust severity 2009 (main season) 2010 (off-season) 1. 1 WC-1#29 TMR 10MR 1. 2 WC-1#32 MRMS 15MSS 1. 3 WC-1#109 RMR 15MRMS 1. 4 WC-2#7 TR 20MRMS 1. 5 WC-2#12 TR 20MRMS 1. 6 WC-2#41 TR 20MR 1. 7 WC-2#80 TR 20MSMR 1. 8 WC-2#98 TR 5MRMS 1. 9 WC-2#100 TMR 10MR 1. 10 WC-3 #15 TMSMR 10MR 1. 11 WC-3 #19 TR 10MRMS 1. 12 WC-4 #12 TR 20MSMR 1. 13 WC-4 #62 TR 20MSMR 1. 14 WC-4 #93 TR 5SMS 1. 15 WC - 12 # 40 TR 15MR 1. 16 WC - 12 #66 TMS 15RMR 1. 17 WC -16 #31 TR 10R 1. 18 WC -16 #37 TR 20RMR 1. 19 WC -16 #57 TR 15MR 1. 20 WC -16 #145 TR 20RMR 1. 21 DW-A- 4 #12 TMR 5RMR 1. 22 DW-A-3 #18 TMR 15MR 1. 23 DW-A-3 #20 TR 20RMR 1. 24 DW-A-3 #70 TR 20MR 1. 25 DW-A-3 #73 TMR 5MS 1. 26 DW-K-1#57 TR 15MR 1. 27 DW-K-1#145 TR 20RMR 1. 28 CD-1-#73 TMR 5MS 29 Yerer TMR 30MRMS 30 Ude 5MR 10MS 31 PBW343 50S 80S In 2010 off-season the stem rust pressure was quite high and only 28 landraces were found to be resistant to stem rust. Those entries showed similar or low levels of stem rust reaction when compared with the resistant durum wheat cultivars namely Yerer and Ude (Table 1). Out of these, 20 belong to those collections from Wollo, two from Kaffa, five from Ambo, and one from Chefe Donsa. The stem rust disease pressure is often high in the off-seasons when compared to the main seasons even without artificial inoculation at Debre Zeit which might be due to favorable (warmer) temperatures in the off- season. Probably that was the reason that accounted for the high pressure of stem rust and low frequency of stem rust resistant landraces in the 2010 off-season compared to the 2009 main season. In this study, combined resistance to stem and leaf rust diseases have been identified in the 28 Ethiopian durum wheat landraces. In previous reports, the Ethiopian durum landraces have been reported to be excellent sources of stem rust (Bechere et al., 2000) and powdery mildew resistance (Negassa, 1986). Furthermore, the importance of Ethiopian tetraploid wheat landraces as sources of resistance to wheat stem rust was reported by Betesellassie et al. (2007). This finding is further supported by the work of Dyck and Sykes (1995) as they found combined resistances to stem and leaf rust in the Ethiopian durum landraces. The Ethiopian durum wheat landrace, ST464 carrying Sr7a, Sr9e and Sr13 genes has been utilized as a source of resistance to stem rust in wheat breeding programs of many countries (Knott, 1996; Klindworth et al., 2007). In this study, 28 durum wheat landraces were found to be resistant to leaf and stem rust of wheat with combined virulence for TTKSK and other races with virulence for Sr13 and Sr9e and the leaf rust races prevailing in Debre Zeit. CONCLUSION The result showed that the Ethiopian durum landraces are potential sources of stem rust resistance and they could be exploited in wheat breeding programs. Figure 1. Frequency (%) of landraces under different leaf rust resistance categories tested at Debre Zeit, 2009 main season (N= LR, 991) Figure 2. Frequency (%) of landraces under different stem rust resistance categories tested at Debre Zeit, 2009 main season (N= SR, 991) Table 1. The reaction of selected durum wheat landraces to the prevailing stem rust races at Debre Zeit in 2009 and 2010 seasons. Valuable Sources of Resistance in the Ethiopian durum wheat landraces to Ug99 and other stem rust races REFERENCES Andenow Y, Hulluka M, Belay G, Tesemma T. 1997. Resistance and tolerance to leaf rust in Ethiopian tetraploid wheat landraces. Plant Breeding 116: 533-536. Bechere E, Kebede H., and Belay G. 2000. Durum wheat in Ethiopia. An old crop in an ancient land. Institute of Biodiversity Conservation and Research (IBCR), Addis Ababa, Ethiopia. 68 p. Bechere E., Tessema T., Huluka M., Andenow Y. 1995. Breeding durum wheat for resistance to leaf and stem rusts in Ethiopia. In: Proceedings of a Regional Workshop for Eastern, Central and Southern Africa. Njoro, Kenya, October 2-6, 1994. Breeding for disease resistance with emphasis on durability. Danial, D. L. (ed.). pp. 125-132. Betessilassie N., Fininsa C., Badebo A. 2007. Sources of resistance to stem rust (Puccinia graminis f.sp. tritici) in Ethiopian tetraploid wheat accessions. Genetic Resources and Crop Evolution 54: 337-343. Brama RN, Sivasamy M, Saikia A. 2003. New wheat lines with superior yield components and resistance to stem, leaf, and strip rust. Annual Wheat Newsletter 49: 48-49. Dyck PL, Sykes EE. 1995. The inheritance of stem rust and leaf rust resistance in some Ethiopian wheat collections. Euphytica 81: 291-297. Haile KJ., Hammer K., Badebo A., Singh RP., Roeder MS. 2012. Haplotype analysis of molecular markers linked to stem rust resistance genes in Ethiopian improved durum wheat varieties and tetraploid landraces. Geneti Resour and Crop Evol. Online Doi.10.1007/s10722-012-9880-0. Huluka M., Andenow Y.1992. Variation within indigenous durum wheat germplasm for response to stem and leaf rust races in Ethiopia. In: The 7 th Regional Wheat Workshop for Eastern, Central and Southern Africa. Nakuru, Kenya, September 16-19, 1991. CIMMYT. Tanner, D. G. and Mwangi, W. (eds.). pp. 131-134. IBC (Institute of Biodiversity Conservation). 2007. Ethiopia: Country Report on the State of Plant Genetic Resources for Food and Agriculture to FAO. 46p. Klindworth DL., Miller JD, Jin Y, Xu SS. 2007. Chromosomal locations of genes for stem rust resistance in monogenic lines derived from tetraploid wheat accession ST464. Crop Science 47: 1441-1450. Knott DR. 1996. The transfer of stem rust resistance from the Ethiopian durum wheat St.464 to common wheat. Canadian Journal of Plant Science 76: 317-319. Negassa M. 1986. Estimates of phenotypic diversity and breeding potential of Ethiopian wheats. Hereditas 104: 41-48. Peterson RF, Campbell AB, Hannah AE. 1948. A diagrammatic scale for estimating rust intensity of leaves and stems of cereals. Canadian Journal of Research 60: 496-500. Pretorius ZA, Singh RP, Wagoire WW, Payne TS. 2000. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Diseases 84:203. Roelfs AP, Singh RP, Saari EE. 1992. Rust diseases of wheat: Concepts and methods of disease management. Mexicco, D.F.: CIMMYT. 81 p.

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INTRODUCTION

Puccinia. graminis f.sp. tritici is one of the debilitating wheat diseases worldwide. For at least two decades, stem rust of

wheat was considered to be a disease of minor importance mainly due to the incorporation of Sr31 resistance gene in

many of the bread wheat cultivars; however, this gene succumbed to a new stem rust race called Ug99 (TTKSK)

(Pretorius et al., 2000). In Ethiopia, two types of wheat (hexaploid, Triticum aestivum L., and tetraploid, T. turgidum L)

are cultivated under rain-fed conditions mainly by resource-poor farmers. Durum wheat (T.turgidum subsp. durum Desf.)

is the predominating tetraploid, which is an indigenous crop in Ethiopia whereas bread wheat is an introduction, and most

of the high yielding semi-dwarf bread wheat varieties are susceptible to Ug99 and other races prevalent in the country. In

the absence of resistance in cultivated varieties, new sources of resistance are sought from landraces and related species.

Ethiopia is endowed with an immense genetic diversity for tetraploid wheat. All the six species of wheat observed by

Vavilov in the mid-1920s are still grown by farmers as landraces (IBC, 2007). The Ethiopian tetraploid landraces have

been identified to be potential sources of disease resistance including stripe and stem rust (Betesellassie et al., 2007; Haile

et al., 2012).

The high level of diversity in these landraces allows breeders and pathologists to make selection for different traits of

economic importance. Therefore, the major objective of this study was to identify sources of resistance in the Ethiopian

durum wheat landraces to Ug99 and other prevailing races of stem rust at Debre Zeit, Ethiopia.

MATERIALS and METHODS

A total of 991 durum wheat landraces collected from different areas of Ethiopia (Tigray, Gondar, Gojjam, Wollo, Shewa

and Kaffa) were used in this study. The collections were made and maintained as single lines by various researchers of

durum wheat improvement program of Debre Zeit Agricultural Research Center. The experiment was conducted in 2009

and 2010 seasons. In 2009 main season, a total of 991 entries were tested whereas in 2010 off-season, 132 landraces

selected from the main season were used. Each entry was planted in two rows of 1m length together with four checks

(PBW343, Morocco, Ude and Yerer). PBW343 is carrying Sr31 gene (Brama et al., 2003), Morocco (susceptible check),

Ude and Yerer are CIMMYT originated commercail durum wheat varieties in Ethiopia. The nursery was bounded by

spreader rows planted with mixtures of susceptible durum (Arendeto and local red) and bread wheat (PBW343) varieties.

The spreader rows were inoculated three times starting from stem elongation with mixtures of TTKSK (Ug99) and other

races carrying virulences for stem rust resistance genes including Sr13 using the injection method (Roelfs et al., 1992).

The rust assessment was made three times using the Modified Cobb’s scale (Peterson et al., 1948). The terminal severity

was used to categorize the entries into resistant and susceptible groups. The severity was converted to coefficient of

infection (CI) values by multiplying the severity by constant values (Roelfs et al., 1992). The constant values are: R= 0.2,

MR=0.4, MS=0.8 and S=1. Based on the CI values, the entries were categorized under four resistant groups: The first

group included the landraces with 0-10% severity (resistant), the second with severity 15-20% (moderately resistant), and

the third with severity of 25-30% moderately susceptible whereas the rest were considered as susceptible. However, only

entries which combined leaf and stem rust resistances were advanced to the next stage of evaluation in 2010 off-season.

Worku Denbel1* and Ayele Badebo2 1 Ethiopian Institute of Agricultural Research (EIAR), Kulumsa Agricultural Research Center, P.O. Box. 489, Asella, Ethiopia 2 Debre Zeit Agricultural Research Center, P.O.Box 32, Debre Zeit, Ethiopia

*Corresponding author: [email protected]

RESULTS and DISCUSSION

In 2009 main season, the leaf rust diseases pressure was quite high, and out of the total entries tested, only 4.8% were

resistant, 13.2% were moderately resistant, 32.9% were moderately susceptible and the remaining 49.1% were

completely susceptible to the disease (Figure 1). Leaf rust has been reported to be the most common disease wherever

durum landraces are grown (Huluka and Andnew, 1992). In this study, almost all of the durum wheat landraces

exhibited susceptible or moderately susceptible reaction to leaf rust; however, they varied in terminal severities. The

absence of complete resistance to leaf rust in the landraces is also in agreement with the previous reports (Andenow et

al., 1997; Huluka and Andenow, 1992). In Ethiopia, durum wheat and stem rust have co-evolved for thousands of

years and this close association has resulted in the accumulation of a wider virulence spectrum on the side of the rust

(Bechere et al., 1995). The use of durum wheat parents with low level of moderately susceptible or moderately

resistant infection types is a valuable and a recommended breeding strategy which has been utilized for durum wheat

improvement in Ethiopia (Bechere et al., 1995) and as a result of such breeding methodology a number of durum

wheat varieties have been released by Debre Zeit Agricultural Research Center.

In 2009 main season, stem rust incidence was relatively low and the highest stem rust severity was 50% on susceptible

varieties. Out of 991 landraces evaluated for stem rust resistance, 79.5% exhibited resistance reaction, 10.6% were

moderately resistant, 8% were moderately susceptible and the remaining 1.9% was completely susceptible (Figure 2).

The low level of stem rust infection was attributed to the susceptibility of many of the landraces to leaf rust which

appeared early in the season. Under such circumstances, it was difficult to select for stem rust resistance under field

conditions since the tissue was being killed by leaf rust at early stages. Therefore, only 132 entries which combine

stem and leaf rust resistances have been selected for the subsequent test.

No. Entries Stem rust severity

2009

(main

season)

2010

(off-season)

1.

1 WC-1#29 TMR 10MR 1.

2 WC-1#32 MRMS 15MSS 1.

3 WC-1#109 RMR 15MRMS 1.

4 WC-2#7 TR 20MRMS 1.

5 WC-2#12 TR 20MRMS 1.

6 WC-2#41 TR 20MR 1.

7 WC-2#80 TR 20MSMR 1.

8 WC-2#98 TR 5MRMS 1.

9 WC-2#100 TMR 10MR 1.

10 WC-3 #15 TMSMR 10MR 1.

11 WC-3 #19 TR 10MRMS 1.

12 WC-4 #12 TR 20MSMR 1.

13 WC-4 #62 TR 20MSMR 1.

14 WC-4 #93 TR 5SMS 1.

15 WC - 12 # 40 TR 15MR 1.

16 WC - 12 #66 TMS 15RMR 1.

17 WC -16 #31 TR 10R 1.

18 WC -16 #37 TR 20RMR 1.

19 WC -16 #57 TR 15MR 1.

20 WC -16 #145 TR 20RMR 1.

21 DW-A- 4 #12 TMR 5RMR 1.

22 DW-A-3 #18 TMR 15MR 1.

23 DW-A-3 #20 TR 20RMR 1.

24 DW-A-3 #70 TR 20MR 1.

25 DW-A-3 #73 TMR 5MS 1.

26 DW-K-1#57 TR 15MR 1.

27 DW-K-1#145 TR 20RMR 1.

28 CD-1-#73 TMR 5MS 29 Yerer TMR 30MRMS 30 Ude 5MR 10MS 31 PBW343 50S 80S

In 2010 off-season the stem rust pressure was quite high and only 28 landraces were found to be

resistant to stem rust. Those entries showed similar or low levels of stem rust reaction when compared

with the resistant durum wheat cultivars namely Yerer and Ude (Table 1). Out of these, 20 belong to

those collections from Wollo, two from Kaffa, five from Ambo, and one from Chefe Donsa. The stem

rust disease pressure is often high in the off-seasons when compared to the main seasons even without

artificial inoculation at Debre Zeit which might be due to favorable (warmer) temperatures in the off-

season. Probably that was the reason that accounted for the high pressure of stem rust and low

frequency of stem rust resistant landraces in the 2010 off-season compared to the 2009 main season.

In this study, combined resistance to stem and leaf rust diseases have been identified in the 28

Ethiopian durum wheat landraces. In previous reports, the Ethiopian durum landraces have been

reported to be excellent sources of stem rust (Bechere et al., 2000) and powdery mildew resistance

(Negassa, 1986). Furthermore, the importance of Ethiopian tetraploid wheat landraces as sources of

resistance to wheat stem rust was reported by Betesellassie et al. (2007). This finding is further

supported by the work of Dyck and Sykes (1995) as they found combined resistances to stem and leaf

rust in the Ethiopian durum landraces. The Ethiopian durum wheat landrace, ST464 carrying Sr7a,

Sr9e and Sr13 genes has been utilized as a source of resistance to stem rust in wheat breeding

programs of many countries (Knott, 1996; Klindworth et al., 2007).

In this study, 28 durum wheat landraces were found to be resistant to leaf and stem rust of wheat with

combined virulence for TTKSK and other races with virulence for Sr13 and Sr9e and the leaf rust

races prevailing in Debre Zeit.

CONCLUSION

The result showed that the Ethiopian durum landraces are potential sources of stem rust resistance and

they could be exploited in wheat breeding programs.

Figure 1. Frequency (%) of landraces under different leaf

rust resistance categories tested at Debre Zeit, 2009 main

season (N= LR, 991)

Figure 2. Frequency (%) of landraces under different

stem rust resistance categories tested at Debre Zeit,

2009 main season (N= SR, 991)

Table 1. The reaction of selected durum wheat

landraces to the prevailing stem rust races at Debre

Zeit in 2009 and 2010 seasons.

Valuable Sources of Resistance in the Ethiopian durum

wheat landraces to Ug99 and other stem rust races

REFERENCES

Andenow Y, Hulluka M, Belay G, Tesemma T. 1997. Resistance and tolerance to leaf rust in Ethiopian tetraploid wheat landraces. Plant Breeding 116: 533-536.

Bechere E, Kebede H., and Belay G. 2000. Durum wheat in Ethiopia. An old crop in an ancient land. Institute of Biodiversity Conservation and Research (IBCR),

Addis Ababa, Ethiopia. 68 p.

Bechere E., Tessema T., Huluka M., Andenow Y. 1995. Breeding durum wheat for resistance to leaf and stem rusts in Ethiopia. In: Proceedings of a Regional

Workshop for Eastern, Central and Southern Africa. Njoro, Kenya, October 2-6, 1994. Breeding for disease resistance with emphasis on durability. Danial, D.

L. (ed.). pp. 125-132.

Betessilassie N., Fininsa C., Badebo A. 2007. Sources of resistance to stem rust (Puccinia graminis f.sp. tritici) in Ethiopian tetraploid wheat accessions. Genetic

Resources and Crop Evolution 54: 337-343.

Brama RN, Sivasamy M, Saikia A. 2003. New wheat lines with superior yield components and resistance to stem, leaf, and strip rust. Annual Wheat Newsletter 49:

48-49.

Dyck PL, Sykes EE. 1995. The inheritance of stem rust and leaf rust resistance in some Ethiopian wheat collections. Euphytica 81: 291-297.

Haile KJ., Hammer K., Badebo A., Singh RP., Roeder MS. 2012. Haplotype analysis of molecular markers linked to stem rust resistance genes in Ethiopian

improved durum wheat varieties and tetraploid landraces. Geneti Resour and Crop Evol. Online Doi.10.1007/s10722-012-9880-0.

Huluka M., Andenow Y.1992. Variation within indigenous durum wheat germplasm for response to stem and leaf rust races in Ethiopia. In: The 7th

Regional Wheat Workshop for Eastern, Central and Southern Africa. Nakuru, Kenya, September 16-19, 1991. CIMMYT. Tanner, D. G. and

Mwangi, W. (eds.). pp. 131-134.

IBC (Institute of Biodiversity Conservation). 2007. Ethiopia: Country Report on the State of Plant Genetic Resources for Food and Agriculture to

FAO. 46p.

Klindworth DL., Miller JD, Jin Y, Xu SS. 2007. Chromosomal locations of genes for stem rust resistance in monogenic lines derived from tetraploid

wheat accession ST464. Crop Science 47: 1441-1450.

Knott DR. 1996. The transfer of stem rust resistance from the Ethiopian durum wheat St.464 to common wheat. Canadian Journal of Plant Science

76: 317-319.

Negassa M. 1986. Estimates of phenotypic diversity and breeding potential of Ethiopian wheats. Hereditas 104: 41-48.

Peterson RF, Campbell AB, Hannah AE. 1948. A diagrammatic scale for estimating rust intensity of leaves and stems of cereals. Canadian Journal of

Research 60: 496-500.

Pretorius ZA, Singh RP, Wagoire WW, Payne TS. 2000. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp.

tritici in Uganda. Plant Diseases 84:203.

Roelfs AP, Singh RP, Saari EE. 1992. Rust diseases of wheat: Concepts and methods of disease management. Mexicco, D.F.: CIMMYT. 81 p.