Printer Friendly

Prospects of Wheat Breeding for Durable Resistance against Brown, Yellow and Black Rust Fungi.

Byline: Aziz Ur Rehman, M.Sajjad, S.H. Khan and Nadeem Ahmad

Abstract

Wheat leaf, stripe and stem rusts have devastating role in reducing crop yield resulting in socio-economic instability many times across the world. The semi-dwarf wheat varieties with race specific resistance could not survive longer due to the evolution of new rust races. However, varieties like Lerma Rojo-64, Yaqui-50 and Lyalpur-73 developed in early part of green revolution retained resistance for longer time due to presence of adult plant resistance (APR) genes. Evolution of new rust races like virulence's Yr9 and Yr27 followed by the emergence of Ug99 and its mutants lead the breeders to revise their breeding strategy. Breeders are now depending on accumulation of minor genes or their use in combination with major genes for durability of rust resistance in wheat varieties. The minor genes/APR genes, Sr2/Yr30, Lr34/Yr18, Lr46/Yr19 are being exploited in wheat breeding at CIMMYT and other places. The germplam with this type of resistance have shown survival consistency over space and time.

At Ayub Agriculture Institute, Faisalabad the home of green revolution in Pakistan, this strategy has been adopted since 1995. The partial resistance varieties were crossed in a top cross/back cross scheme and the segregating populations were advanced by selected bulk method, which resulted in the development of material having better yield and rust resistance than the pre-exiting varieties (e.g., Inqlab-91, MH-97). Three varieties, Shafaq-06 and Lasani-08 and AARI-11 from these crosses have been approved for general cultivation. Similarly, the material developed and distributed by CIMMYT, Mexico having this type of resistance is being globally adopted. The SSR markers for above mentioned minor genes are available and can be used as an aid in the early selection of superior genotypes. (c) 2013 Friends Science Publishers

Keywords: Durable resistance; Rust; Wheat; Breeding

Introduction

Wheat along with rice and maize is fulfilling half of the calories demands of the human population around the world. The projected global wheat production for the year 2009-2010 is 656 million tones, which is slightly higher than the demand of 642 million tones. Global Wheat production has increased tremendously since green revolution in 1960's and helped in minimizing hunger and malnutrition. Developing countries, which consume 60% of the global wheat production, have shown higher yield increase than the developed countries in the past (Heisey et al., 2002).

It was driven by the hunger prevalence in these countries and is attributable to the introduction of high yielding and rust resistant semi dwarf varieties developed under the collaborative efforts of International and National research systems during last 50 years. Whereas, climate change and emergence of new pests and diseases are threatening the food sustainability. The evolution of new races of pathogens like Ug 99 of stem rust are of serious concern. In order to feed the ever growing population increase in wheat production at the rate 1.6% can be achieved by developing high yielding varieties having good tolerance level for biotic and abiotic stresses.

Wheat rusts have major historical and economic importance worldwide. Yield losses due to rusts had been reported in many wheat producing countries in most years and periodic epidemics during last century resulted in famine situation in many parts of the world (Brennan and Murray, 1988). The control of rust diseases of wheat in Australia has been estimated to save farmers income over $ 200 million annually (Brennan and Murray, 1988). The yield losses due to black rust (Puccinia graminis f. sp. tritici) were independently reported by Italian scientists Fontana and Tozzeti in the 18th century. The rusts affect the photosynthetic ability of the plant and transportation of photosynthates from green part of the plant, which results shriveled grains (Fig. 1). This adversely affects the yield, moreover, the grain quality is also badly affected resulting lower price in market. Therefore, to sustain wheat productivity and farmers income some strategies must be adopted to control these menaces.

In developed countries the use of chemicals is common for controlling rusts but it is unaffordable by the poor farmers of Africa, Asia and other developing countries. The only way left unblocked is the development of rust resistant stock, which had been the major breeding strategy since the early 1900's.

Genetic manipulation of resistance genes has resulted in more stable pattern of resistance (Macindoe and Brown, 1968; Lupton, 1987; Singh and Dubin, 1997) and helped in feeding ever increasing world population. It has been estimated that wheat genetic improvement has generated at least 27 times its value in benefits from leaf rust (brown rust) resistance breeding in spring wheat alone (Marasas et al., 2004).

After the birth of Mendelian Genetics in the beginning of 20th Century, Biffen (1905) demonstrated that inheritance of wheat yellow rust (stripe rust), caused by Puccinia striiformis f. sp. tritici (Pst) followed Mendelian principles. After devastating rust epidemics in North America in the early part of 20th century, Stalkman and Piemeisel (1917) demonstrated that stem rust pathogen has various forms and races. These races varied in their ability to be virulent on different wheat varieties which were later found to carry distinct resistant gene or gene combinations. Flor (1942,1956) demonstrated that incompatibility between host and pathogen involved corresponding genes in each organism. This consideration of gene for gene relationship led to the development of following two fundamental rules parallel to basic Mendelian Principles by Loegring in 1966 justified by McIntosh et al. (1995), and stated as: a).

Incompatibility between host and pathogen is the consequence of interaction between the products of at least one host resistant and at least one corresponding pathogen avirulence gene: LIT=LP:LR.

LIT is low infection type, LP is low pathogenicity, and LR is low reaction.

b). When more than one interacting gene pairs are involved the level of incompatibility as low as, or lower than, the level produced by the most incompatible interacting gene pair acting alone, that is: LIT1,2 less than L1T1 where:LIT1 less than L1T2.

Wheat Breeding in Pre-green Revolution Era

There was no serious attempt in wheat improvement until the early years of 19th century. Twenty five types (T1-T25) belonging to T. durum, T. Sphaerococum and T. vulgare (T. aestivum) were isolated from the mixture of genotypes and species (Aziz, 1966; Rehman et al., 2009). The mixture of genotypes was commonly known as landraces, which evolved as a result of natural selection and some times assisted by farmers own selection of better heads for the seed of next year crop. These landraces remained under cultivation until the first decade of 20th century (Rehman et al., 2009). Main breeding method used by the breeders of nineteenth century was isolation of pure lines from local land races following Johnson's pure line theory. Hybridization in most part of the world was started by the end of nineteenth century. Some crosses had also been reported to be made to combine contrasting characters of parents in hybrid varieties.

Farrer (1898), in Australia, gave due consideration for breeding rust resistant wheat varieties. He carefully selected the parents for hybridization work and mainly concentrated on the development of early maturing varieties to avoid rusts. He also imported some early maturing germplasm from India and crossed with Australian material. He used back cross approach for introgression of rust resistance into Australian material. He listed as components of rust resistance: size of stomata, presence of leaf wax, thickness of cuticle, leaf angle (erect leaves offering a less suitable site for spore deposition) and leaf width. These characteristics are remarkably similar to those now considered likely to determine durable disease resistance. He also developed interspecific crosses of wheat with T. monococcum (Einkorn) for transferring rust resistance in wheat.

In India these crosses were imported during 1896-1901 but could not acclimatize in Indian conditions and wheat land races or their derivatives mostly predominated. Some varieties of sub-continent like Mundia, Pissi, Bansi, Nagpur hybrid, Bakhshi, Majhi were found moderately resistant but not immune (Howard and Howard, 1909), which indicated that they may posses few minor genes for rust resistance. As the main breeding method used for the development of wheat varieties in those days was isolation of pure lines, therefore, it can be assumed that these minor genes were co-evolved with the bread wheat.

In Russia, scientific breeding dates back to 1902 but early work was confined to the selection from local or introduced populations. Hybridization with collected wild and cultivated forms from areas of primitive agriculture for introgression of alien alleles was also conducted in this part of the world. Their interest in wide crosses is clearly shown by the parentage of famous variety Besostaja and its derivatives Aurora and Kavkaz. The variety Kavkaz had shown wide adaptability in different climatic conditions (Lupton, 1987) and was used extensively as a donor of rust resistance genes all over the world.

In spring wheat areas of North America, varieties released since early days of breeding have adult plant resistance or combination of adult plant resistance and seedling resistance. The varieties Webster, Ceres and several Hope and H-44 derivatives are typical examples of adult plant resistance. Other varieties released were combination of adult plant resistance of one parent and seedling resistance of the other parent: an example is New- Thatcher. Another method called analytical in those days was also used, which targets combining partial resistance of two or more varieties to develop rust resistant varieties (da Silva, 1958; Knott, 1958). Lupton (1987) revealed that in North America the history of spring wheat breeding after the 1916 black rust epidemic showed the rise and fall of many varieties carrying major gene, each displaced following the spread of rust race virulent to their respective genes.

A major advancement followed the introduction of variety Selkirk in 1954, which maintained its resistance for more than 25 years and appeared to carry factors for durable resistance in addition to major gene resistance for which it was originally selected.

In Germany, some early winter wheat hybrids varieties such as Strube-56 and Carstens-5 with good level of field resistance were developed in 1934. In Indian sub-continent, then it was considered that no further development was possible through pure line selection and therefore, hybridization was started for breeding still better varieties in 1926 (Aziz, 1966), by combining all maximum desirable characters in a variety present in more than one types. The varieties including C-591, C-518, C-217, C-250, C-271 and C-273 were developed by crosses using local and exotic germplasm. These varieties were superior to pre-existing stock in all respects. The variety C271 contains Lr34 (Kolmer, 2009), a durable rust resistance gene. This showed that this gene has been used in wheat breeding consciously or unconsciously since long.

So it can be concluded that in the early days of wheat breeding, although the knowledge regarding genetics of rust resistance was not much advanced but due consideration was given for the selection of varieties having better resistance. Many selections from land races also possessed good resistance (30-40M). After the establishment of hybridization programs, varieties with adult plant resistance (race non-specific resistance) and race-specific resistance were developed. The varieties, developed with race specific resistance, were not long-living therefore, development of varieties with adult plant resistance (APR) remained the effective breeding strategy. Sometimes breeder accumulated APR genes, while targeting a major gene, which gave their varieties long life. Some inter-specific crosses were also developed for introgression of alien genes in wheat genome.

Green Revolution and Breeding for Rust Resistance

The semi-dwarf and dwarf varieties developed at CIMMYT, Mexico in the early days of green revolution (Penjamo 62, Pitic 62, Lerma Rojo 64, Sanora 64 and Siete Cerros etc.) had been responsible for yield breakthrough in Pakistan, India, Turkey, Afghanistan and many other parts of the world. The life time of most of these Mexican varieties was short as appearance of new stem rust race has terminated their useful life time however, there were some exceptions also. The variety Lerma Rojo 64 had life time of eleven year, while others like Yaqui 50, Champingo 52 and Champingo 53 retained their resistance until they were displaced from commercial cultivation by new high yielding varieties (Borlauge, 1968). The long life of these varieties is attributable to their genetic background. They had combination of Hope and Thacher type and Kenya type resistance (Borlauge, 1958). During the period 1965-1985, the CIMMYT wheat breeding program has incorporated diversity of genes.

Most of the material distributed during this period contains Sr2 and two to four additional genes for stem rust resistance (Table 1). These additional genes include Sr5, Sr6, Sr7a, Sr7b, Sr8a, Sr9b, Sr9d, Sr9e, Sr9g, Sr10, Sr11, Sr12, Sr17, Sr24, Sr26, Sr30, Sr31, Sr36 (Green and Dyck, 1979; Rajaram et al., 1988; Knott, 1988). The parallel strategy was also adopted by many national programs.

The importance of Lr13 gene for leaf rust (Puccinia triticina) resistance was recognized in the early 1970's when it was transferred along with other genes into many wheat varieties. Some varieties containing Lr13 in combination with other genes developed in Mexico, India and Pakistan are given in Table 2. The gene, Lr13 itself does not provide desired level of resistance but when present in combination with other genes it provides a degree of resistance of high probability of being durable. The mode of action of Lr13 complex in CIMMYT program is non race- specific resistance. Its presence in combination with Lr34 in some members of Bluebird series gave them long life. Another example of this combination is a Pakistani variety Lyalpur 73 (Fig. 2), which although replaced in the farmers field by the introduction of new high yielding varieties but even after 36 years of release, it still has very good resistance for leaf rust (20M) in screening nurseries.

The varieties like Genero 81 and Torim 73, which remained resistant to leaf rust in Mexico for long time also have Lr 34 gene in combination with other genes.

The adult plant resistance to leaf rust of the Brazilian wheat cultivar "Frontana" was first described as due to the gene Lr13 (effective in the adult plant stage) and one or two modifiers (Dyck et al., 1966). Subsequent studies (Dyck and Samborski, 1982; Dyck, 1987) revealed the presence of Lr 34 and Lr13 in "Frontana". Pretorius et al. (1984) showed that Lr13 could confer low seedling reaction at elevated temperature. The gene Lr13 appears to be common in cultivars from Australia (Hawthorn, 1984); India (Gupta and Saini, 1987); and Brazil, Argentina and Unites States (Roelfs, 1988); and in cultivars derived from CIMMYT germplasm (Singh and Rajaram, 1991).

The interaction of Lr13 with other genes such as Lr16 and Lr34 have also been reported (Dyck and Samborski, 1982; Ezzahiri and Roelfs, 1989).

The interaction of Lr13 with other Lr genes has been considered as the cause of durable resistance to leaf rust in many cultivars (Rajaram et al., 1988; Roelfs, 1988). Singh and Rajaram (1992) investigated the inheritance of adult plant resistance in "Frontana" and 3 globally leaf rust resistant CIMMYT spring bread wheat varieties, the genetic test for the presence of Lr34, the postulation of the other known Lr genes, and the role of Lr13 and other known Lr genes in conferring adult plant resistance. They concluded that resistance was independent of major genes.

The material developed during mid 1960's had acquired resistance for yellow rust from Andean region varieties which possessed high level of resistance. The Anza was derived from cross LR/N10B//3ANE and released in North Africa, Sudan, South Africa and New Zeland.

Table 1: Stem rust resistance genes in old wheat varieties (after McIntosh et al., 1995)

Varieties###Year of release###Country/Region###Genes

Selkirk###1954###Canada###Sr2,Sr6,Sr7b,Sr9d,Sr17

Hope###1927###USA###Sr2,Sr7b,Sr9d,Sr17

Newthach###-###USA###Sr2,Sr5,Sr7b,Sr12

Lerma Rojo 64###1964###Mexico###Sr2,Sr6,Sr7b,Sr9e

Penjamo T 62###1962###Mexico###Sr5,Sr6,Sr8a, Sr9b

Kenya Plume###-###Kenya###Sr2, Sr5, Sr6, Sr7a, Sr8a , Sr12, Sr17

Maxipak###1965###Pakistan###Sr17

Kalyansona###India

Sonalika###1967###India###Sr2

Bluesilver###1971###Pakistan

Bluebird###1976###Mexico###Sr2, Sr5, Sr6, Sr8a

Yecora 70###1975###Pakistan

PARI 73###1973###Pakistan

Nuri 70###1975###Pakistan

Pavon F 76###1976###Mexico###Sr2, Sr8a, Sr12, Sr30

Hartog###1983###Australia###Sr2, Sr8a, Sr9g, Sr30

Songlen###1975###Australia###Sr2, Sr5, Sr6, Sr8a, Sr36

Qing Chung 5###-###China###Sr5, Sr6, Sr11

Hochzucht###-###Eurpian Union###Sr5, Sr9g, Sr12

Karl###1988###USA###Sr2, Sr9d , Sr24

Frontana###1943###South America###Sr8a, Sr9b

Sunco###2006###Australia###Sr5, Sr6, Sr8a, Sr24, Sr36

Sunelg###1984###Australia###Sr24, Sr26

Table 2: Leaf rust resistance genes in old wheat varieties as described by McIntosh et al. (1995)

Varieties###Year###Country/Region###Genes

Lerma Rojo###1964###Mexico###Lr13, Lr17

Champingo 53###1953###Mexico###Lr34

Penjamo 62###1962###Mexico###Lr14a, Lr34

Pitic62###1962###Mexico###Lr14a

Sonora64###1964###Mexico###Lr1

Mexipak 65###1965###India###Lr 14a

Kalyansona###Pakistan

Sonalika###1967###India###Lr13,Lr14a

Bluesilver###1971###Pakistan

Lyalpur 73###1973###Pakistan###Lr1,Lr13,Lr34

Bluebird###1976,###Mexico###Lr1,Lr13, Lr34

Yecora 70###1975###Pakistan

PARI 73###1973###Pakistan

Nuri 70###1975###Pakistan

Ciano 79###1979###Mexico###Lr16

Arz###1973###Lebnon###Lr17

Pavon F 76###1976###Mexico###Lr1, Lr10, Lr13, Lr 46

Hortog###1983###Australia

Dollarbird###1987###Australia

Parula###1981###CIMMYT###Lr34, Lr46

Punjab 81###1981###Pakistan###Lr10, Lr13, Lr34

Era###1970###North America###Lr10, Lr13, Lr34

Frontana###1943###South America###Lr13,Lr34

Chines Spring###-###China###Lr12, Lr34

Bezostaya###-###Europe###Lr3a, Lr34

Hobbit###-###UK###Lr13, Lr17

Singh et al. (1998)

It was regarded as durable resistant for yellow rust by Johnson (1988) and may have derived durable resistance from Anderson (Rajaram et al., 1988). Durable resistance of Anza is widely deployed in spring wheat and in some winter wheat varieties. This durable resistance was attributed to the presence of gene Yr18 by Singh (1992a). The varieties, developed in early days of green revolution, carrying Yr18 are given in Table 3. The gene, Yr7 is also present in a range of spring wheat and winter wheat varieties and it is frequently associated with Sr9g. It is reported in number of varieties such as Barani 83, PBW12, WL2265, Seri 82 (Yr2, Yr7, Yr9), Pavon76 (Yr6, Yr7, Yr29), Pak. 81(Yr7,Yr9) (Dubbin et al., 1989; Perwaiz and Johnson, 1986; Wellings 1986; Badebo et al., 1990; Singh et al., 1990). It is usually present in many cultivars as a combination as mentioned in Table 3.

Veery and Pavon containing Yr7 had been released in 31 and 16 countries, respectively with different names (Table 4, 5), which show the wide use of Yr7 gene.

Table 3: Yellow rust resistance genes in old wheat varieties (McIntosh et al., 1995)

Varieties###Year###Country/ Region###Genes

Lerma Rojo###1964###Mexico###Yra

Champingo 53###1953###Mexico###Yr 18

Sonalika###1967###India###Yr2,YrA,

Lyalpur 73###1973###Pakistan###Yr 18

Bluebird###1970###Mexico###Yr6, YrA, Yr18,

Pavon F 76###1976###Mexico###Yr6,Yr7,Yr29

Hortog###1983###Australia

Dollarbird###1987###Australia

Ciano79###1979###Mexico###Yr Sulkirk (Yr 27)

Veery###1980,S###Worldwide###Yr7,Yr9

Barani 83###1983###Pakistan###Yr7

PBW343 (Attilla)###1995###India###Yr Sulkirk (Yr 27)

Inqilab 91###1991###Pakistan###Yr Sulkirk (Yr 27)

Era###1970###North America###Yr 18

Frontana###1943###South America###Yr 18

Chines Spring###-###China###Yr 18

Bezostaya###-###Europe###Yr 18

Singh et al. (1998)

Table 4: Derivatives of Veery (CM 33027- KVZ/BUH//KAL/BB) released in different parts of the world (Skovmand et al., 1997)

Country###Varieties

Bangladesh###SERI 82- BGD

Bolivia###CHANE CIAT

Brazil###BR26-SAO GOTARDO, BR31-MIRITI, IAC 289-MARRUA, IAPAR28-IGAPO, OCEPAR 18

Chile###MILLALEAU INIA, NOBO INIA, SNA 204, SNA 205, SNA 206, SNA 210

China###GOU JI 13, JING XUAN 9, YUN ZHI 437

Egypt###GIZA 164

Ethiopia###DASHEN, HAR 407

Guatemala###ICTA OLINTEPEQUE 86

India###HS 207, HUW206, MACS2496,MALAVIYA206

Iran###FALAT

Lebanon###SERI 82-LBN

Libya###BOHOOTH 202

Mexico###GENARO T 81, GLENNSON M 81, SERI M 82, URES T 81

Morrocco###TILILA

Myanmar###YEZIN WHEAT 6

Nepal###ANNAPURNA 1, NL 459

Pakistan###PAK 81, PIRSABAK 85, MEHRAN 89

Paraguay###CORDILLERA 3

Peru###LA MOLINA 82

Portugal###LIMA 1, TAMEGA

Rawanda###GICINYA

South Africa###GAMTOOS

Spain###ARGANDA, CARTHAYA

Sudan###SASARAIB

Tanzania###TAUSI, VIRI

Turkey###ANADOLU, KAKLIC 88, SERI 82-TUR

Uaaan###NARRO F.86

Uruguay###ESTANZUELA CARDENAL

Yemen###AZIZ, MUKHTAR

Zambia###LOERIE, LOERIE II, SERIC

Zimbabwe###NATA, RUSAPE, SCW 101

1B-1R Translocation

Driscoll and Sear (1965) and Sears (1967) produced several lines having a translocation between a segment of hairy neck chromosome of rye 5R and different wheat chromosome segments. Due to genetic relationship between rye chromosome 5R and wheat chromosome of homology group 1, the designation 1R was proposed for this chromosome (Shephered, 1968, 1973; Shephered and Jennings, 1971). The rye chromosome 1R was reported to be containing powdery mildew and stripe rust resistance genes in its short arm (Riley and Macer, 1966). It was found that these genes were linked with stem rust and leaf rust resistant genes and cultivars Salzmunder, Baertweizen and Weique have identical genes (Bartos and Bares, 1971).

A sister line of these ,,Neuzutch' was used for breeding in Soviet Union and gave rise to Russian cultivars Kavkaz, Aurora, Besostaya 2, Skorospelka and many others.

Table 5: Details of parents selected and utilized in gene pyramiding crosses at AARI, Faisalabad-Pakistan

Varieties/Lines###Characteristics

###Leaf rust###Yellow rust###Av. Yield (Kg/ha)

Inqilab-91###20M###70S###4000-4500

V-87094(Wattan)###40M###40M###4000-4500

Kohistan-97###30M###50M###4000-4500

Luan###30M###40M###3000

MH-97###50MSS###60MSS###4000-4500

Shalimar-88###60M###40M###3500-4000

Punjab-96###40S###40M###4000-5000

Weaver###20M###10MR###3000

S=susceptible, MS moderately susceptible, MR Moderately resistance

M moderately resistant moderately susceptible

Table 6: Yield performance of selected durable rust resistant elite lines of AARI, Faisalabad- Pakistan

Line###Parentage###trials Testing years###Av. Yield (Kg/ha)###Check (Inqilab)###% inc./ dec over check

V-00183R (Shafaq-06)###V87094/2 Inq-91###120###5###4110###4031###+2.70

V-02192###SH88/V87094//MH97###124###5###4049###3970###+2.44

V-02156###SH-88/Weaver###50###4###4236###4046###+4.5

V-03007###Pb96/V87094//MH97###37###4###4505###4288###+5.06

V-04179###Pb96/V87094//MH97###37###4###4658###4488###+4.7

V -03138###Luan/Koh.97###125###3###4141###3983###+3.96

Table 7: Potential rust reactions of finally selected elite lines of AARI, Faisalabad at hot spots in Pakistan

Line###Parentage###Leaf rust###Yellow rust

###Bahwalpur###Faisalabad###Islamabad###Pirsabak

V-00183R (Shafaq-06)###V87094/2 Inq-91###0###0###10MR###20MR

V-02192###SH88/V87094//MH97###0###20M###10R###5RMR

V-02156###SH-88/Weaver###5MR###40MS###10RMR###20RMR

V-7096###Pb96/V87094//MH97###5MRMS###30MRMS###10R###40RMR

V-04179###Pb96/V87094//MH97###0###40M###10R###40RMR

V -03138###Luan/Koh.97###10MR###30M###5R###15MR

Mumtaz#1###LU26/PRL// LU26/TRAP###10MR###5R###5M###10MR

Mumtaz#2###LU26/PRL// LU26/TRAP###15M###20M###10M###20M

Morrocco###100S###100S###100S###100SN

Neuzutch possesses a complete 1R chromosome, whereas Kavkaz and Aroura have an interchange chromosome having 1B segment and a rye chromosome 1R segment. (Mettin et al., 1973; Zeller, 1973; Zeller and Hossam, 1983). Kavkaz was introduced into CIMMYT germplasm where a high yielding spring wheat cultivar "Veery" was released.

This segment was also transferred to several Europian cultivars. These cultivars were found possessing resistance to wheat streak mosaic virus and its vector wheat curl mites. There was good compensation of Rye chromosome 1R for the elimination of wheat chromosome 1B. The 1B.1R translocation appears to be more stable and superior in agronomic properties. It was easy for the breeders to work with this translocation as there was no cytological problem associated with it (Zeller and Hossam, 1983). Therefore, this translocation became widespread in wheat cultivars released in China and USA, India, Pakistan and several other countries during the mid-1980s and later. The Veery derivatives due to their superior agronomic feature and disease resistance were widely cultivated in different parts of the world (Table 4).

This germplasm showed significant grain yield advantage and wide adaptation with superior disease resistance attributes due to the presence of the 1B-1R translocation. The higher yielding ability of 1B-1R germplasm was attributed to post-anthesis stress tolerance of this material resulting in higher Kernal weight (Morenosevilla, 1995). The frequency of 1B.1R translocation went up to approximately 70% at one stage in CIMMYT's spring wheat germplasm but has declined to about 30% in more recent advanced lines (Singh et al.,2006; Rehman et al., 2013). Introgression of 1B-1R translocation and wide spread adoption of the material carrying it on global basis, probably enhanced the emergence of new devastating races like Yr9, Yr27 virulence's of yellow rust and stem race Ug 99.

Although the genes Sr31, Lr26 and Yr9 present in this translocation remained effective for long period of time but their breakdown forced the scientist to devise some alternative strategy of gene deployment in wheat varieties for rust resistance.

This translocation, derived from imperial Rye carries genes Sr31, Lr26, Yr9 and Pm8. (Zeller and Hossam, 1983; McIntosh et al., 1995), when used initially it provided resistance to stem rust, leaf rust and yellow rust but with the development of new virulent races, these genes are in- effective now (Singh et al., 2006). Despite, its successful use it was not widely deployed in Australia due to sticky dough, poor mixing characteristics resulting poor bread making qualities (Roelfs, 1988; McIntosh et al., 1995; Rehman et al., 2013).

Emergence of New Rust Races

The wide spread global popularity of the germplasm with 1B-1R translocation created monoculture situation. This lead to the evolution of some new devastating rust races resulting a serious threat to global wheat production. A race of P. striiformis, Yr9 was 1st observed in East Africa in 1986 and subsequently migrated to North Africa and South Asia. Once it appeared in Yemen in 1991 it took just four years to reach wheat fields of south Asia (Singh and Huerta-Espino, 2000). On its way it caused major yield losses in Egypt, Syria, Turkey, Iran, Iraq, Afghanistan and Pakistan exceeding USD 1 billion. Similarly, Yr27 emergence and its movement following the same pathway posed major threat to wheat production in India and Pakistan, where mega cultivars PBW343 and Inqilab-91 were having Yr27 gene based resistance. In 2005, the wheat crop in Nothern Pakistan was severely hit by this race of Yellow rust where most of the area was under Inqilab-91.

Stem rust resistance in wheat cultivars with Sr31 remained effective for more than 30 years. In 1990's, most of the wheat varieties were having 1B-1R translocation which created a monoculture situation in Africa, Asia and other parts of the world. Isolates of pgt, which were virulent on Sr31 were collected for the 1st time in Uganda during 1999 and then spread throughout East Africa (Pretorius et al., 2000). It subsequently spread to Kenya and Ethiopia in 2005 (Waynera et al., 2006). The race, named as TTKS (Ug99), is virulent on majority of mega wheat varieties and can cause 100% yield losses whereas, up to 80% yield losses have been reported in Kenya. A new variant of this stem rust race has been found in Kenya since 2006, which is virulent on Sr24 (Jin et al., 2007, 2008). Now-a-days fungicides are being used to control stem rust in Kenya (Singh et al., 2008). It ultimately jumped the red sea and its presence has been reported in Yemen since 2006 and was also found in Sudan in the same year.

In March 2007, isolates of pgt were collected from different locations in Iran and the collections from Borujerd and Hamadan were identified as TTKSK (Nazari et al., 2009). The race identified, produced high IT's of 3 to 4 on wheat genotypes carrying 1BL-1Rs translocation (Falat and PBW343).

Subsequently, FAO announced its existence in Iran and alarmed a threat for, the bread-basket zone of the world, South Asia and other neighboring regions.

A new race of stem rust virulent on Sr25 gene, have been detected in India (Jain et al., 2009). This isolate collected from Karnataka, has shown IT's 3+ to 4 on primary leaves of differential types with Sr25 gene. This race is named as PKTSC according to North American system. The detection of Sr25 virulent race alarmed the breeders that they should breed for adult plant resistance or pyramid 2 or 3 major genes to enhance the field life of wheat cultivars.

Durable Rust Resistance

The problem of ever changing races of pathogens led the breeders to evolve alternative forms of resistance that would be more durable such as slow rusting or partial resistance (Broers, 1989; Singh et al., 2000a, b). It has been demonstrated that durable rust resistance is more likely to be of adult plant type rather than of seedling type and is not linked with the genes producing hypersensitive reaction (McIntosh, 1992; Bariana et al., 2001). Durable rust resistance is a mechanism conferring resistance to a cultivar for long period of time during its widespread cultivation in a favorable environment for a disease (Johnson, 1978, 1988). This type of resistance is mainly associated with the minor genes, which are also known as slow rusting genes. The concept of slow rusting in wheat was recommended by Caldwell (1968), analogous to partial resistance to late blight of potato proposed by Niederhauser et al. (1954).

Many researchers have emphasized the need to identify and exploit durable resistance. Johnson and Law (1975) defined durable resistance as a resistance source that remained effective after widespread deployment over a considerable period. A general concept of a durable resistance source for cereal rusts is that it is polygenic, likely to express at adult plant stage, non-race-specific and produce non-hypersensitive response to infection. A typical example of durable resistance is the resistance to stem rust transferred from tetraploid emmer to North American bread wheat cultivars Hope and H-44 (Hare and McIntosh, 1979), and resistance to leaf rust in the South American wheat cultivar Frontana (Rajaram et al., 1988).

Genetic Basis of Durable Resistance

The durable resistance is based on additive effect of partial resistant minor genes, usually polygenic in nature and active in adult plant stage. Genetic studies conducted at CIMMYT, Mexico has shown that at least 10-12 different genes are involved in group of CIMMYT germplasm, and by accumulating 4-5 minor genes resistance level near to immunity can be achieved. However 2-3 genes in a line provide moderate level of resistance (Singh et al., 2005). Most of these genes are undesignated only the genes Lr34/ Yr18, Lr46/Yr29 and Sr2/Yr30 have been given names and designated to specific chromosomes. Each of these genes pairs are tightly linked or pleotropic.

The varieties possessing minor gene based resistance show almost same level of resistance over space and time. For example Lyalpur-73, which was among major varieties of Pakistan in 1970's still show very good level of resistance in screening nurseries (Fig. 2). Whereas, the varieties having

Table 8: Comparison of leaf rust reaction of varieties having minor gene based resistance in Maxico and Pakistan

Variety/Line###Minor Genes possessed###Usual rust reactions

###Mexico###Pakistan

Nacozari 76###Lr34+1###30MSS###30M

Sonoita###Lr34+1###20MSS###10M

Baconora 88###Lr34+1 or 2###10MSS###20M

Frontana###Lr34+ 2 or 3###10MSS###15M

Trap#1###Lr34+ 2 or 3###10MSS###20M

Kukuna###Lr34+ 3 or 4###1M###5MR

Parula###Lr34+Lr46+1or 2###10MS###10M

Pavon 76###Lr46+1###30MS###40M

Amadina###4###5M###10M

Table 9: Comparison of leaf rust reaction reactions of some varieties having minor gene based resistance in Mexican and Pakistani conditions

Variety/Line###Minor genes possessed###Usual rust reactions

###Mexico###Pakistan

Pavon 76###Yr29+Yr30+1###40M###30M

Parula###Yr18+Yr29+Yr30+1###10M###20M

Kukuna###Yr18+ 3-4###10MR###TR

Trap#1###Yr18+2###10MR###20M

Amadina###Yr29+Yr30+1###30M###20M

Kakatsi###3-4###10MR###5M

major gene based race specific resistance did not have long life and collapsed usually after 4-5 years. Varieties having durable type of resistance show almost same level of reaction against different races and their resistance remained effective in different climatic conditions. The leaf rust and yellow rust reaction of some varieties having durable rust resistance are same at CIMMYT, El Batan, Mexico and Faisalabad, Pakistan (Table 8, 9). The variety Frontana being released about half century ago still have effective rust resistance almost every where. There are very rare examples that resistance based on major genes had been effective for a longer period of time. William et al. (2006) identified 6 independent loci, contributing to adult plant resistance (APR) or slow rusting contributing to two rusts in a population derived from cross of Avocet ,,S' and Pavon.

The putative loci influencing resistance to stripe and yellow rust were identified on chromosomes 1BL, 4BL and 6AL. The loci on chromosome 3BS and 6BL had significant effect on stripe rust. In another population a locus on the distal region of chromosome 1BL was identified with highly significant effects on stripe rust resistance (Bariana et al., 2001; Suenaga et al., 2003). Even Morocco and Avocet S have some genetic factors that contain some slow rusting resistance which results in significant delay in becoming completely susceptible (William et al., 2006). The material having minor gene based resistance near to immunity ( less than 10M) for leaf and yellow rust was developed and distributed worldwide in 1990's by CIMMYT (Singh et al., 2000a).

Sr2/Yr30 Gene

The gene, Sr2 was transferred to hexaploid wheat from

Fig. 1: Grano-gram showing grain shriveling at various intensity levels of stem rust

Fig. 2: Field life of wheat varieties in Pakistan

tetraploid emmer wheat cultivar Yaroslav in 1920. It is present on chromosome 3BS (Hare and McIntosh, 1979) and is also reported to be associated with Lr27 (Singh and McIntosh, 1984). It is completely linked with pseudo black chaff (Pbc), which is used as morphological marker for identification of lines carrying this gene. The genotypes with Pbc show varying level of stem rust infection. The maximum severity level of 60-70% has been noted as compared to 100% severity of susceptible check in disease screening nurseries in Kenya. When present alone it does not provide sufficient level of resistance but in combination with other genes desirable level of resistance can be achieved. Much information is not available about the interaction of Sr2 and other genes in Sr2 complex. The adequate resistance level can be achieved by accumulating 4-5 minor genes (Knott, 1988).

Sr2 was detected in several highly resistant old, tall Kenyan cultivars like Kenya plume (Singh and McIntosh, 1986) and semidwarf CIMMYT, cultivars Pavon F 76, Parula, Kingbird, Dollarbird etc. These cultivars show maximum disease severity of 10-15% with moderately resistant reactions. The gene Sr2 is tightly linked with Yr30 or has pleotropic effects (Singh et al.,2000b).

A microsatellite (SSR) marker gwm533 is tightly linked and associated with the presence of this gene, which can be used to facilitate selection of this difficult to score gene (Spielmeyer et al., 2003).

Lr34/Yr18: A number of genes conferring resistance to rusts have been identified and used in wheat (T. aestivum L.) breeding programs. However, many of these genes have become ineffective because of the emergence of new virulent races of rusts. Cultivars such as Frontana with the rust resistance gene Lr34 had operative durable rust resistance to leaf rust (P. triticina) (Dyck et al., 1966; Singh and Rajaram, 1992). Although Lr34 has been used extensively in spring wheat grown in US, isolates of P. tiriticina with complete virulence to this gene had not been identified, therefore, the resistance in Frontana might be due to escape from a complete virulent leaf rust race (Kolmer et al., 2003). It has been reported that soft red winter wheats having Lr34 in combination with seedling resistant Lr2a, Lr9, Lr26 were highly resistant, whereas, in combination with Lr10, Lr11, Lr18 were moderately to low resistant in USA (Kolmer, 2009).

A major leaf rust resistance gene Lr34 first described by (Dyck, 1977, 1987) has been established to improve leaf rust resistance in combination with other genes (German and Kolmer, 1992). Another salient characteristic of Lr34 resistance is that it is genetically tightly linked with Yr18 gene, which confers adult plant resistance (Singh, 1992a, b; McIntosh, 1992). This gene co-segregates with leaf tip necrosis (Ltn1), powdery mildew resistance (Pm38), Barley yellow dwarf virus (Bydv1) genes (McIntosh, 1992; Singh et al., 1992a, b, Spielmeyer et al., 2005; Liang et al., 2006). These multi-pathogen resistance traits have made the Lr34/Yr18 locus one of the highly valuable regions for disease resistance in wheat (Kolmer et al., 2008). If Lr34/Yr18 complex is present alone the disease level may go high but in combination with other genes it could give effective control (Ma and Singh, 1996).

At low temperature the resistance level conferred by plants with Lr34 is higher under growth chamber and green house condition. The gene seems to be effective under field conditions at average daily temp 0-20C and helps in reducing disease progress (McIntosh et al., 1995). Singh and Rajaram (1991) had indicated that environment has a significant influence on terminal disease reaction for leaf rust. Singh (1992b) showed that Yr18 may display inadequate resistance under some environmental conditions. It is present in many sub- continental varieties including some released in pre-green revolution era. A marker associated with csLV34 locus on chromosome 7D was found associated with Lr34/Yr18 gene. Two predominant allelic size variants csLV34a and csLV34b were identified. A strong association was observed with the presence Lr34/Yr18 gene and csLV34b allele. However, lines having Lr34/Yr18 gene and positive for csLv34a allele were rare.

The lineage of this gene is tracked back to varieties Mentana and Ardito developed in Italy during early 1990's (Kolmer et al., 2008). This gene has been cloned and was shown that Lr34/Yr18/Pm38/Ltn1 is the same gene (Krattinger et al., 2009).

Lr46/Yr29: A slow rusting gene identified in the cultivar Pavon and was found located on chromosome 1B by crossing with a monosomic series of adult plant leaf rust susceptible cultivar Lal Bahadur (Singh et al., 1998a). This is the 2nd named minor gene involved in slow rusting. The leaf rust resistance gene Lr46 and yellow rust resistance gene Yr29 are tightly linked or pleotropic (William et al., 2003).

Its effect is similar to Lr34/Yr18 as it does not provide complete immunity to plants. Infected adult plants carrying Lr46 have longer latency period as compared to control without this gene (Martinez et al., 2001). The plants with this gene also show higher rate of fungal colonies abortion with out any chlorotic or necrotic effects and also decrease the colony size. The resistance conferred by this gene is not of hypersensitive type. Suenaga et al. (2003) determined that the microsatellite locus Xwmc44 is located 5.6-cM proximal to the putative QTL for Lr46. Leaf tip necrosis (Ltn) has been reported to be highly correlated with the presence of Lr46/Yr29 (Rosenwarne et al., 2010) and efforts are underway to clone this gene (www.ars.usda.gov).

Combining Minor Genes

Accumulating minor genes for attaining desired level of resistance in a variety is a challenging task (Singh and Trethewan, 2007) as it requires identification of parents with minor genes, crossing them in specific schemes following back cross or top cross approach, maintaining desirable population size and selection of desirable genotypes from segregating populations. The crossing schemes and selections strategies used for breeding major genes based resistance are not suitable for breeding minor gene resistance. The modified pedigree method used for breeding major gene based resistance can not give any progress for minor gene based resistance. Singh et al. (1998b) compared different crossing and selection schemes for working out their efficiency in terms of genetic gains and cost efficiency. The influence of type of cross and selection scheme was minimal on main grain yield. They found that selection of parents was the most important feature in breeding for achieving desirable results.

They also reported that mean rust severity of top cross progenies was less as compared to simple cross because two parents contributed resistance factors to the top cross progenies. Non selected bulk method was found to be least effective and selected bulk method as the most attractive schemes in terms of genetic gain and cost efficiency. An example of breeding for minor gene based resistance is the development of wheat stock resistant to leaf and yellow rust at CIMMYT.

Since early days of breeding for minor genes, plants and lines with infection intensity of 20-30% and compatible infection type were targeted. This led to the development of wheat varieties Nacozari F 76, Pavon F 76 and several others (Singh and Trethewan, 2007), which were released not only in Mexico but also in Ethiopia, Bangladesh, Pakistan and other countries. Pavon was released in 16 countries with different names (Table 5). This material provided the foundation for breeding for minor gene resistance. In Pakistan the varieties Uqab-2000 (CROW'S'/NAC/BOW'S'), Bhakkar-02 (P- 102/PIMA//F3.71/TRM/3/PVN) and Seher-06 (CHIL/2 STAR/BOW/CROW//BUC/PVN/3/VEE#10) have this type of resistance. Bhakkar-2002 has dominated the mega wheat cultivar Inqlab-91 since 2005 after Inqlab-91 was hit by yellow rust epidemic and Seher-06 is gaining popularity now, due to its higher yield and better resistance to leaf and yellow rusts.

The variety, Uqab-2000 proved the best option for the rain- fed northern Pakistan after severe epidemic of yellow rust in 2005.

An example of breeding for durable rust resistance out side CIMMYT is the wheat breeding program of Ayub Agricultural Research Institute, Faisalabad-Pakistan. The collection of 1200 accessions was screened under artificial inoculation with mixture of all prevailing rust races in Pakistan like Yr9, Yr27, Lr10, Lr13, Lr26 virulences etc. The accessions (Table 6) with partial resistance for leaf/yellow rust were selected (Hussain et. al., 2006). The selected parents were crossed to combine genes for high yield and rust resistance. The major objective was the accumulation of minor genes for longer-lasting rust resistance. The selected parents were used to create back crosses, double crosses and top crosses. Bulk selection as described by Singh et al. (2005), was used to advance the filial generations conserving maximum genetic diversity. The spikes were harvested from the plants having rust intensity ranging 0-30% preferably with R/MR/MS type of reaction.

Many lines were selected from this material and tested for yield and disease reaction (Table 6, 7). From this material two varieties Shafaq-06 and Lasani-08 with durable resistance based on unknown minor genes were accepted for general cultivation in the Punjab-Pakistan (Hussain et al., 2007; 2009). These varieties are high yielding and have shown durable resistance to leaf and yellow rust races like Yr9, Yr27, Lr10, Lr13, Lr26 virulences etc. Lasani-08 was also found resistance to stem rust (Ug 99) in the year 2007 at Kenya.

Conclusion

The ever changing nature of wheat leaf, stripe and stem rusts poses a serious threat to future wheat production. Learning from wheat breeding history and epidemic losses by wheat rusts, breeders devised the strategy of pyramiding APR/minor genes. The strategy of pyramiding APR genes was developed by understanding rust resistance mechanism prevalent in historical wheat varieties like Lerma Rojo-64, Yaqui-50 and Lyalpur-73 which retained resistance due to then unknown APR genes. CIMMYT and AARI devised a strategy of pyramiding APR genes alone or in combination with major genes to combat the recently emerged races of stem and yellow rust. Recent wheat cultivars bred at AARI, Faisalabad such as Shafaq-06, Lasani-08 and AARI-11 are strong evidences of potential of APR gene pyramiding strategy to cope with threats of leaf, stripe and stem rusts.

Reference

Aziz, M.A., 1966. Cereals and Pulses, Resume of Fifty Years Research Work at Punjab Agricultural College and Research Institute, Lyallpur. Department of Agriculture, West Pakistan Badebo, A., R.W. Stubbs, M. van-Ginkel and G. Gebeyehu, 1990.

Identification of resistant genes to Puccinia striformis in seedlings of Ethiopian and CIMMYT bread wheat varieties and lines. Netherlands J. Plant Pathol., 96: 199-210

Bariana, H.S., M.J. Hayden, N.U. Ahmad, J.A. Bell, P.J. Sharp and R.A. McIntosh, 2001. Mapping of durable adult plant and seedling resistance to stripe and stem rust disease in wheat. Aust. J. Agric. Res. 52: 1247-1255

Bartos, P. and I. Bares, 1971. Leaf and stem rust resistance of hexaploid wheat cultivars, Salzmunder, Bartweizen and Weique. Euphytica, 20: 435-440

Biffen, R.H., 1905. Mendel's laws of Inheritance and wheat breeding. J. Agric. Sci., 1: 4-48

Borlauge, N.E., 1958. The use of multilineal or composite varieties to control airborn epidemic diseases of self pollinated crops. In: Proc. 1st Int. Wheat Genet Symp., pp: 12-27. University of Manitoba, Canada

Borlauge, N.E., 1968. Wheat breeding and its impact on world food supply In: 3 Int. Wheat Genet Symp., pp: 1-36. Canberra, Australia

Brennan, J.P. and G.M. Murray, 1988. Australian wheat diseases assessing their economic importance. Agric. Sci., 2: 26-35

Broers, L.H.M., 1989. Partial resistance to wheat leaf rust in 18 spring wheat cultivars. Euphytica, 44: 247-258

Caldwell, R.M., 1968. Breeding for general and/or specific plant disease resistance. In: Proc. Third Int. Wheat Genet Symp., pp: 263-272. Canherra, Australia

da Silva, A.R., 1958. The introgression of wheat breeding and rust identification. In: Proc. First Int. Wheat Genet Symp., pp: 39-48. University of Manitoba, Canada

Driscoll, C.J. and E.R. Sears, 1965. Mapping of wheat rye translocation. Genetics, 51: 439-443

Dubbin, H.J., R. Johnson and R.W. Stubbs, 1989. Postulated genes for resistance to stem rust in selected CIMMYT and related wheats. Plant Dis., 73: 472-475

Dyck, P.L., 1977. Genetics of leaf rust resistance in three introductions of common wheat. Can. J. Gent. Cytol., 19: 711-716

Dyck, P.L., 1987. The association of a gene for leaf rust resistance with the chromosome 7D suppressor of stem rust resistance in common wheat. Genome, 29: 467-469

Dyck, P.L. and D.J. Samborski, 1982. The inheritance of resistance to Puccinia recondita in a group of common wheat cultivars. Can. J. Genet. Cytol., 24: 273-283

Dyck, P.L., D.J. Samborski and A.G. Anderson, 1966. Inheritance of adult plant resistance derived from the common wheat varieties Exchange and Frontana. Can. J. Genet. Cytol., 8: 665-671

Ezzahiri, B. and A.P. Roelfs, 1989. Inheritance and expression of adult plant resistance to leaf rust in Era wheat. Plant Dis., 73: 549-551

Farrer, W., 1898. The making and improvements of wheats for Australian conditions. Agric. Gaz. NSW, 9: 131-168; 241-260

Flor, H.H., 1942. Inheritance of pathigenesity in Melampsora lini. Phytopathology, 32: 653-659

Flor, H.H., 1956. The complementary genic system in flax and flax rust. Adv. Genet., 8: 29-54

German, S.E. and J.A. Kolmer, 1992. Effect of gene Lr 34 on the enhancement of resistance to leaf rust of wheat. Theor. Appl. Genet., 84: 97-105

Green, G.J. and P.L. Dyck, 1979. A gene for resistance to Puccinia graminis f.sp. tritici that is present in wheat cultivar H-44 but not in cultivar Hope. Phytopathology, 69: 672-675

Gupta, A.K. and R.G. Saini, 1987. Frequency and effectiveness of Lr13 in conferring wheat leaf rust resistance in India. Curr. Sci., 56: 417-419

Hare, R.A. and R.A. McIntosh, 1979. Genetic and cytogenetic studies of durable adult plant resistance in Hope and related cultivars to wheat rusts. Z. Pflanzenzuchtung, 83: 350-367

Hawthorn, W.M., 1984. Genetic analysis of leaf rust resistance in wheat. Ph.D. Thesis, University of Sydney, Australia

Heisey, P.W., 2002. International Wheat Breeding and Future Wheat Productivity in Developing Countries. Wheat year book/ WHS 2002. Economic research activities/USDA

Howard, A. and G.L.C. Howard, 1909. Wheat in India: Its Production, Varieties and Improvement: The Empirical Dept. Agric. India. Thacker, Spink and Co., Calcutta, India

Hussain, M., N. Ayub, S.M. Khan, M.A. Khan, F. Muhammad and M. Hussain, 2006. Pyramiding rust resistance and high yield in bread wheat. Pak. J. Phytopathol., 18: 11-21

Hussain, M., M. Hussain, A. Rehman, F. Muhammad, M. Hussain, M. Zulkiffal, N. Ahmad, N. Ahmad and M.A. Khan, 2009. Lasani-08, a new wheat variety with minor gene based rust resistance. Pak. J. Phytopathol., 21: 152-158

Hussain, M., A. Rehman, M. Hussain, F. Muhammad, M. Younis, A.Q. Malokra and M. Zulkiffal, 2007. A new high yielding durable rust resistant variety Shafaq-06. Pak. J. Phytopathol., 19: 238-242

Jain, S.K., M. Prashar, S.C. Bhardwaj, S.B. Singh and Y.P. Sherma, 2009. Emergence of virulence to Sr25 of Puccinia graminis f. sp. tritici of wheat in India. Plant Dis., 93: 480

Jin, Y., Z.A. Pretoriou and R.P. Singh, 2007. New virulence within race TTKS(Ug99) of the stem rust pathogen and effective resistant genes. Phytopathology, 97: 137-140

Jin, Y., L.J. Sczabo, Z. Pretorius, R.P. Singh and T. Fetch, 2008. Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis., 92: 923-926

Johnson, R., 1978. Practical breeding for durable resistance to rust diseases in self pollinating cereals. Euphytica, 27: 529-540

Johnson, R., 1988. Durable resistance to yellow (stripe) rust in wheat and its implications in plant breeding. In: Breeding Strategies for Resistance to the Rusts of Wheat, pp: 63-75. Simmonds, N.W. and S. Rajaram (eds.). CIMMYT, Mexico

Johnson, R. and C.N. Law, 1975. Genetic control of durable resistance to yellow rust (Puccinia striiformis) in the wheat cultivar Hybride de Bersee. Ann. Appl. Biol., 81: 385-391

Knott, D.R., 1958. The inheritance of stem rust resistance. In: Proc. First Int. Wheat Genet Symp., pp: 32-38. University of Manitoba, Canada Knott, D.R., 1988. Using polygenic resistance to breed for stem rust resistance in wheat. In: Breeding Strategies for Resistance to the Rusts of Wheat, pp: 39-47. Simmonds, N.W. and S. Rajaram (eds.). CIMMYT, Mexico

Kolmer, J.A., 2009. Postulaton of leaf rust resistant genes in selected soft red winter wheats. Crop Sci., 43: 1266-1274

Kolmer, J.A., D.L. Long, E. Kosman and M.E. Hughes, 2003. Physiological specialization of Puccinia triticiana on wheat in the United States in 2001. Plant Dis., 87: 859-866

Kolmer, J.A., R.P. Singh, D.F. Gravin, L. Vicaars, H.M. William, J. Huerta-Espino, F.C. Ogbonnayya, H. Raman, S. Orford, H.S. Bariana and E.S. Lagudha, 2008. Analysis of Lr34/Yr18 rust resistance region in wheat germplasm. Crop Sci., 48: 1841-1852

Krattinger, S.G., E.S. Lagudah, W. Spilmeyer, R.P. Singh, J. Huerta- Espinno, H. McFadden, E. Bossolini, L.L. Selter and B. Keller, 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 323: 1360-1363

Liang, S.S., K. Savenaga, Z.H. He, Z.L. Wang, H.Y. Liu, D.S. Wang, R.P.

Singh P. Sourdille and Y.C. Xia, 2006. Quantitative trait loci mapping for adult plant resistance to powdery mildew in bread wheat. Phytopathology, 96: 784-789

Lupton, F.G.H., 1987. History of wheat breeding. In: Wheat Breeding, its Scientific Basis, pp: 51-70. Lupton, F.G.H. (ed.). Chapman and Hall, London

Ma, H. and R.P. Singh, 1996. Contribution of adult plant resistant gene Yr 18 in protecting wheat from yellow rust. Plant Dis., 80:66-69

Macindoe, S.L. and C.W. Brown, 1968. Wheat Breeding and Varieties in Australia. Science Bulletin 76, NSW Department of Agriculture, Australia

Marasas, C.N., M. Smale and R.P. Singh, 2004. The Economic Impact in Developing Countries of Leaf Rust Resistance Breeding in CIMMYT Related Spring Wheat. Economic program paper, 04-01, CIMMYT, Mexico DF, Mexico

Martinez, F., R.E. Nicks, R.P. Singh and D. Rubiales, 2001. Characterization of Lr46, a gene conferring partial resistance to wheat leaf rust. Hereditas, 135: 111-114

McIntosh, R.A., 1992. Close genetic linkage of genes conferring adult-plant resistance to leaf rust and stripe rust in wheat. Plant Pathol., 41: 523-527

McIntosh, R.A., C.R. Wellings and R.F. Park, 1995. Wheat Rusts: An Atlas of Resistant Genes. CSIRO Publication, Australia

Mettin, D., W.D. Bluethner and G. Schlegel, 1973. Additional evidence on spontaneous 1B/1R wheat rye translocation. In: Fourth Int. Wheat Genet Sympo., pp: 179-184. Columbia, Missouri, USA

Morenosevilla, B., P.S. Baenziger, C.J. Peterson, R.A. Graybosch and D.V. Mcvey, 1995. The 1bl. Crop Sci., 35: 1051-1055

Nazari, K., M. Mafi, A. Yahyoui, R.P. Singh and R.F. Park, 2009. Detection of wheat stem rust (Puccinia graminis f. sp. tritici) race TTKSK (Ug99) in Iran. Plant Dis., 93: 317

Niederhauser, I.S., J. Cervames and L. Servin, 1954. Late blight in Mexico and its implications. Phytopathology, 44: 406-408

Perwaiz, M.S. and R. Johnson, 1986. Genes for resistance to yellow rusts in seedlings of wheat cultivars from Pakistan tested with British isolates of Puccinia striformis. Plant Breed., 97: 289-296

Pretorius, Z.A., R.P. Singh, W.W. Wagoire and T.S. Payne, 2000. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis., 84: 203

Pretorius, Z.A., R.D. Wilcoxcan, D.L. Long and D.F. Schaffer, 1984. Detecting wheat leaf rust resistance gene Lr13 in seedlings. Plant Dis., 68: 585-588

Rajaram, S., R.P. Singh and E. Torres, 1988. Current approaches in breeding wheat for rust resistance. In: Breeding Strategies for Resistance to Rusts of Wheat, pp: 101-118. Symmonds, N.W. and S. Rajaram (eds.). CIMMYT, Mexico D.F., Mexico

Rehman, A., M. Sajjad, S. H. Khan, R. J. Pena, N. I. Khan, 2013. Lower Tendency of Allelic Variation of Glu Genes and Absence of 1BL-1RS Translocation in Modern Pakistani Wheats. Cer. Res. Commun., in press Rehman, A., M.A. Khan, F. Muhammad, N. Ahmed and M. Hussain, 2009.

Review of wheat breeding in Punjab-Pakistan. http://www.globalrust.org Riley, R. and R. Macer, 1966. The chromosomal distribution of the genetic resistance of rye to wheat pathogen. Can. J. Genet. Cytol., 8: 640-653

Roelfs, A.P., 1988. Resistance to leaf and stem rusts in wheat. In: Breeding Strategies for Resistance to Rusts of Wheat, pp: 10-22. Symmonds, N.W. and S. Rajaram, (eds.). CIMMYT, Mexico Rosenwarne, G., R.P. Singh, W. William, J. Huerta-Espino, 2010.Identification of phenotypic and molecular markers associated with slow rusting resistance gene Lr46. In Proc: 11th Int. Cereal Rusts and Powdry Mildew Conference. Abstract 1.36

Sears, E.R., 1967. Induced transfer of hairy neck from rye to wheat. Z.P. Flanzenzutchtg, 57: 4-25

Shephered, K.W., 1968. Chromosomal control of endosperm protein in wheat and rye. In: Proc. Third Int. Wheat Genet. Symp., pp: 86-96. Canberra, Australia

Shephered, K.W., 1973. Homeology of wheat and alien chromosomes controlling endosperm protein phenotypes. In: Proc. Fourth Int. wheat Genet. Symp., pp: 745-760

Shephered, K.W. and A.C. Jennings, 1971. Genetic control of rye endosperm proteins. Experienta, 27: 98-99

Singh, H., R. Johnson and D. Seth, 1990. Genes for race specific resistance to yellow rust (Puccinia striiformis) in Indian wheat cultivars. PlantPathol., 39: 424-433

Singh, R.P., 1992a. Genetic association between gene Lr34 for leaf rust resistance and leaf tip necrosis in bread wheats. Crop Sci., 32: 874-878

Singh, R.P., 1992b. Genetic association of leaf rust resistance gene Lr34 with adult plant resistance to stripe rust in bread wheat. Phytopathology,82: 835-838

Singh, R.P. and R.A. McIntosh, 1984. Complementary genes for resistance to Puccinnia recondita tritici in Triticun aestivum L. Genetics and linkage studies. Can. J. Genet. Cytol., 26: 723-735

Singh, R.P. and R.A. McIntosh, 1986. Genetics of resistance to Puccinia graminis tritici and Puccinia recondita tritici in Kenya Plume wheat. Euphytica, 35: 245-256

Singh, R.P. and S. Rajaram, 1991. Resistance to Puccinnia recondita f. sp. tritici in 50 Mexican bread wheat cultivars. Crop Sci., 31: 1472-1479

Singh, R.P. and S. Rajaram, 1992. Genetics of adult plant resistance of leaf rust in ,,Frontana' and three CIMMYT wheats. Genome, 35: 24-31

Singh, R.P. and H.J. Dubin, 1997. Sustainable Control of Wheat Diseases in Mexico. Memorias de 1er Simposio Internacional de Trigo, 7-9 April 1997, cd Obregon, Sanora, Mexico, CIMMYT

Singh, R.P. and J. Huerta-Espino, 2000. Global Monitoring of Wheat Rusts and Assessment of Genetic Diversity and Vulnerability of Popular Cultivars. Research Highlight of CIMMYT wheat program: 1999-2000, CIMMYT, Mexico

Singh, R.P., J. Huerta-Espino and S. Rajaram, 2000a. Achieving near- immunity to leaf and stripe rusts in wheat combining slow rust resistance genes. Acta Phytopathalog. Entomol. Hung., 35: 133-139

Singh, R.P., J.C. Nelson and M.E. Sorrells, 2000b. Mapping Yr28 and other genes for resistance to stripe rust in wheat. Crop Sci., 40: 1148-1155

Singh, R.P., D.P. Hodson, J. Huerta-Espino, Y. Jin, P. Najau, R. Wanyera, S.A. Harrera-Fossil and R.W. Ward, 2008. Will stem rust destroy the world's wheat crop. Adv. Agron., 98: 271-308

Singh, R.P., D.P. Hodson, Y. Jin, J. Huerta-Espino, M. Kinyua, R. Wanyera, P. Najau and R.W. Ward, 2006. Current Status, Likely Migration and Strategies to Mitigate the threat to Wheat Production from Race Ug99 (TTKS) of Stem Rust Pathogen, pp: 1-13. CAB Reviews: Prospectives in Agricultue, Veterinary Sciences, Nutrition and Natural resources 1,54

Singh, R.P., J. Huerta-Espino and H.M. William, 2005. Genetics and breeding of durable resistance to leaf and stripe rusts in wheat. Turk. J. Agric., 29: 121-127

Singh, R.P., A. Mujeeb-Kazi and J. Huerta-Espino, 1998a. Lr46: a gene conferring slow rusting resistance to leaf rust in wheat. Phytopathology, 88: 890-894

Singh, R.P., S. Rajaram, A. Miranda, J. Huerta-Espino and E. Autrique, 1998b. Comparison of two crossing and four selection schemes for yield traits, slow rusting resistance to leaf rust in wheat. In: Wheat: Prospects for Global Wheat Improvement, pp: 93-101. Braun, H.J. (ed.). Kluwer Academic Publishers, Netherland

Singh, R.P. and R. Trethewan, 2007. Breeding spring wheat for irrigated and rainfed production systems of the developing world. In: Breeding Major Food Staples, pp: 109-140. Kang, M.S. and P.M. Priyadarshan (eds.). Blackwell Pub Ltd, UK

Spielmeyer, W., R.A. McIntosh, J. Kolmer and E.S. Lugdah, 2005. Powdry mildew resistance and Lr34/Yr18 genes for durable resistance to leaf and stripe rust, co segregate at a locus on the short arm of chromosome 7D of wheat. Theor. Appl. Genet., 111: 731-735

Spielmeyer, W., P.J. Sharp and E.S. Lagudah, 2003. Identification and validation of markers linked to broad spectrum stem rust resistance gene Sr2 in wheat (Triticum aestivum L.). Crop Sci., 43: 333-336

Stalkman, E.C. and F.J. Piemeisel, 1917. A new strain of P.graminis. Phytopathology, 7: 73

Suenaga, K., R.P. Singh, J. Huerta-Espino and H.M. William, 2003. Microsattelite markers for gene Lr34/Yr18 and other quantitative trait loci for leaf rust and stripe rust resistance in bread wheat. Phytopathology, 93: 881-889

Waynera, R., M.G. Kinyua, Y. Jin and R.P. Singh, 2006. The spread of stem rust caused by Puccinia graminis sp. tritici with virulence on Sr31 in wheat in Eastern Africa. Plant Dis., 90: 113

Wellings, C.R., 1986. Host:Pathogen studies of wheat stripe rust in Australia. Ph.D. Thesis, University of Sydney, Australia

William, H.M., R.P. Singh, J. Huerta-Espino, S. Ortiz-Islas and D. Hoisington, 2003. Molecular Marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust gene Yr29 in wheat.Phytopathology, 93: 153-159

William, H.W., R.P. Singh and G. Palacios, 2006. Characterization of genetic loci conferring adult plant resistance to leaf rust and stripe rust in spring wheat. Genome, 49: 977-930

Zeller, F.J. and S.L.K. Hossam, 1983. Broadening the genetic variability of cultivated wheat by utilizing rye chromatin. In: Proc. Sixth Int. Wheat Genet Symposium, pp: 161-174. Koyoto, Japan

Zeller, F.J., 1973. IB-1R. Wheat rye chromosome substitution and translocation. In: Proc. Fourth Int. Wheat Gent. Symposium, pp: 209-221. Sears, E.R. and L.M.S. Sears (eds.). University of Missouri, Columbia, USA

Wheat Research Institute, AAARI, Faisalabad, Pakistan

Deaprtment of Plant Breeding and Genetics, University of Agriculture, Faisalabad, Pakistan

Center of Agricultural Biochemistry and Biotechnology, University of Agriculture, Faisalabad, Pakistan

For correspondence: aziz_kml@yahoo.com; msajjadpbg@gmail.com
COPYRIGHT 2013 Asianet-Pakistan
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2013 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Rehman, Aziz Ur; Sajjad, M.; Khan, S.H.; Ahmad, Nadeem
Publication:International Journal of Agriculture and Biology
Article Type:Report
Geographic Code:9PAKI
Date:Dec 31, 2013
Words:9969
Previous Article:Evaluation of Genetic Diversity of Raya (Brassica juncea) through RAPD Markers.
Next Article:Improving Drought Tolerance in Maize (Zea mays) with Potassium Application in Furrow Irrigation Systems.
Topics:

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters