Abstract
Various biotic and abiotic stress factors affect plant growth and yield of bread wheat (Triticum aestivum L) . Wheat relatives from Triticeae tribe represent a source of disease resistance and abiotic stress tolerance genes as well as genes increasing grain quality for improvement of bread wheat. Broadening the genetic diversity of bread wheat using alien germplasm is a relevant task in cereal genetics and breeding. The allohexaploid structure of bread wheat genome allows for the construction and maintenance of variably stable material in which a whole chromosome, chromosome arm or its smaller part is replaced by those of a related species via hybridization process. The development of effective and usable DNA markers has made the process of heterologous gene transfer within the Triticeae tribe more efficient. In this chapter, recent advances in wheat improvement via alien gene transfer are briefly reviewed with emphasis on disease resistance.
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Keywords
- Bread wheat
- Triticum
- Aegilops
- Secale
- Triticeae
- Genetic diversity
- Wheat improvement
- Resistance genes
- Fungal diseases
Introduction
Broadening the genetic diversity for economically important traits is one of the main tasks of wheat genetics and breeding. There are many evidences of low allelic variability or loss of alleles related with yield, grain quality, and resistance to biotic and abiotic stresses among modern bread wheat varieties (Fu and Somers 2009; Gultyaeva 2012; Novoselskaya-Dragovich et al . 2015 ). The reduction in genetic diversity was accelerated in the second half of the 20th century, when a replacement of local wheat germplasm on high-yielding commercial cultivars took place. This has been demonstrated by analysis of pedigrees, phenotypic and molecular genetic assessments of plant material ( Dreisigacker et al . 2004; Khlestkina et al. 2004).
Fungal diseases are among the major constraints that affect plant growth and yield of bread wheat (Triticum aestivum L.). Many efforts are focused on transfer of disease resistance genes from various cereal species of Triticeae tribe to the bread wheat genome.
T. aestivum belongs to one of the four Triticum genus sections—the Triticum section consisting of hexaploid wheat species with genome BAuD. Further section (Dicoccoides) is represented by tetraploid emmer wheats with genome BAu, and includes tetraploid progenitor of bread wheat, which hybrized with Aegilops tauschii Coss (genome D), resulting in formation of allohexaploid wheat (BAuD) about 10,000 years ago. Other Triticum sections are Monococcum (diploid einkorn wheat with genomes Au and Ab) and Timopheevi (tetraploid and hexaploid wheat species with genomes GAu and GAuAb, respectively) (Goncharov 2002). Both the B and the G genomes are related to the S genome present in Ae. speltoides (Kimber 1974).
High similarity between Ae. tauschii and T. aestivum D-genome and the close evolutionary relationship between the B, S and G genomes allows for the relatively straightforward transfer of genetic information from Ae. tauschii, Ae. speltoides and T. timopheevii to bread wheat. Further Triticeae species (from Aegilops, Secale and Hordeum genera) also represent an important genetic reservoir for improvement of bread wheat (Friebe et al. 1996; Schneider et al. 2008; Trubacheeva et al . 2008 ; Pershina et al. 2009 ; Molnar-Lang et al. 2014). A wide range of wheat-alien lines has been developed over the past decades (Friebe et al. 1996, 2001; Wheat Genetics Resource Center). Synthetic wheats or lines with translocations and chromosome substitutions are often used as intermediate forms for gene transfer to varieties. The development of effective and usable genetic markers has made the process of heterologous gene transfer within the Triticeae tribe more efficient (Marais et al. 2001; Adonina et al. 2012; Chen et al. 2013; Timonova et al. 2013 ).
A number of resistance genes to leaf, stem, and yellow rusts and powdery mildew has been transferred into the genome of common wheat from wild and cultivated wheat relatives. Successful examples include the transfer of the Lr9 and Lr19 genes from Ae. umbellulata and Th. ponticum species (McIntosh et al. 1995) . Until recently these genes remained effective against a broad set of leaf rust races (Puccinia triticina Eriks.) worldwide.
However, only a small number of the resistance genes described to date are used in breeding for development of resistant wheat varieties. Mainly this is due to the negative effects of foreign genetic material on agronomic traits.
In addition to wide application of alien germplasm for improvement of bread wheat resistance to fungal diseases, genes of various Triticeae species can be useful for increasing bread wheat tolerance to unfavorable environment conditions (reviewed in Colmer et al. 2006; Nevo and Chen 2010; Inbart-Pompan et al. 2013; recent examples are given in Yudina et al. 2015a, b ), improvement of bread making quality ( Aegilops ssp . genes : Kunert et al. 2007; Rehman et al . 2008 ; Garg et al . 2009 ; Sin et al . 2011; Wang et al . 2012 , 2013 ; Zhou et al. 2014; T. dicoccoides Kunert et al. 2007 ) and nutrition properties : various Triticum ssp. and Aegilops ssp . genes can be used for increased production of iron and zink (Rawat et al. 2009) or antioxidant compounds (Khlestkina et al . 2010 ; Tereshchenko et al . 2012a, b ).
Triticum Species for Bread Wheat Improvement
Hexaploid Wheats T. Spelta and T. Macha (BAuD)
Hexaploid wheat T. spelta contributed to bread wheat resistance against septoria tritici blotch via substitution of chromosomes 2D, 5A, 5D, 6B, 6D and 7D (Simon et al. 2005). Two regions of chromosome 7D from spelt wheat were associated with isolate-specific resistance expressed at the seedling (locus QStb.ipk-7D1) and another at the adult (QStb.ipk-7D2) plant stage (Simon et al. 2010). The locus QStb.ipk-7D2 was found on the short arm of chromosome 7D in a similar position to the locus Lr34/Yr18 known to provide durable resistance against multiple pathogen races (Spielmeyer et al. 2008). Substituted chromosome 6B of hexaploid wheat T. macha is a carrier of a major determinant of head blight resistance , chromosomes 2A, 2B, 3A , 4A, 5A and 5B have also positive effect on resistance to these pathogens (Grausgruber et al. 1998 ; Steed et al . 2005; Buerstmayr et al. 2011; Burt et al . 2015 ).
Tetraploid Wheats T. Dicoccoides and T. Durum (BAu)
Powdery mildew resistance genes were transferred from T. dicoccoides to bread wheat chromosomes 6AL (Xie et al. 2003) and 5BL ( PmAS846; Xue et al. 2012). Other genes conferring resistance to this disease were found in T. dicoccoides chromosomes 5BL (Pm36; Blanco et al . 2008 ), 3BL (Li et al . 2009 ) , 2BL (Maxwell et al. 2010) and 2BS (Hua et al. 2009; Liu et al. 2012 ) .
T. dicoccoides leaf rust (Lr53) and stripe rust ( Yr35) resistance genes were transferred to bread wheat chromosome 6BS (Marais et al. 2005 ). Other genes for stripe rust resistance were found in T. dicoccoides ( YrH52 and Yr15, Peng et al . 2000; Yr36 , Uauy et al . 2005 ).
This species is also a potential donor of Fusarium head blight resistance genes (Hartel et al . 2004; Buerstmayr et al. 2013).
T. durum is a perspective donor of stem rust resistance gene Sr13 (Simons et al . 2011 ). The role of Sr13 and the role of chromosome regions putatively harboring Sr9, Sr14, Sr17 and Sr28 was shown for resistance to highly virulent stem rust race Ug99 (Letta et al . 2013 ).
T. durum resistance genes are often transferred to bread wheat via synthetic hexaploid forms obtained by crossing T. durum with Ae. tauschii. Genome-wide association study of 181 synthetic hexaploid wheats revealed a number of stripe rust resistance loci, including that on chromosomes of the A and B genomes of T. durum: 1AS, 1BS, 2AS, 2BL, 3BL, 5A, 5BL, and 7AL (Zegeye et al. 2014).
Molecular analysis of hybrid lines derived from crossing of Belarusian wheat varieties with T. durum suggested contribution of chromosomes 4B and 5B in the formation of the complex resistance to leaf rust, powdery mildew and septoriosis (Leonova et al. 2013 ).
Tetraploid Wheat T. Timopheevii (GAu)
T. timopheevii was a donor of two stem rust resistance gene: Sr36 and Sr37 (McIntosh et al. 2013) . The gene Sr36 (formerly SrTt1) was used in breeding programs for more than 40 years. Sr36 refers to a group of the genes, providing effective resistance to the most aggressive race of stem rust, Ug99 (Yu et al. 2014). For Sr36 gene protocols for polymerase chain reaction were developed and diagnostic markers were designed for application in marker-assisted selection (MAS) programs.
The gene Sr37 (SrTt2) despite its effectiveness against Ug99 was not used in breeding to improve the resistance of wheat varieties because of the significant negative effects of T4BL-4GL translocation on the productivity traits (McIntosh et al. 1995) .
Two genes determining resistance to powdery mildew, Pm6 and Pm27, were transferred from T. timopheevii ssp. timopheevii into chromosomes 2B and 6B respectively (Jørgensen and Jensen 1973 ; Järve et al. 2000 ). The gene Pm6 was widely used for creation of resistant wheat varieties and is still one of the most effective genes in many regions of the world, including Europe, China and North America (Alam et al. 2011) .
Three resistance genes with different efficiency to leaf rust (Lr18, LrTt1, and LrTt2), and two quantitative trait loci (QLr.icg-1A, QLr.icg-2B) were described in the genome of different subspecies of T. timopheevii (Yamamori 1994; Leonova et al. 2007 , 2011 ). The gene Lr18, originating from T. timopheevii ssp . timopheevii has lost its efficacy against leaf rust races worldwide and is not currently used in breeding. The presence of the genes LrTt1 and LrTt2 (T. timopheevii var. viticulosum) and locus QLr.icg-2B (unknown subspecies of T. timopheevii) in wheat genotypes provides resistance to the wide range of leaf rust races in West Siberian regions of Russia (Leonova et al. 2007; Timonova et al. 2013). These loci have been used for creation of breeding lines and wheat cultivar “Pamyati Maistrenko ” (Laikova et al. 2013 ).
Additionally , three genes determining resistance to leaf rust (Lr50), stem rust (Sr40) and powdery mildew (Pm37) were identified in the genome of wild subspecies T. timopheevii ssp. armeniacum (Brown-Guedira et al. 2003; Perugini et al. 2008; Wu et al. 2009) .
Besides the aforementioned genes , there were evidences that wheat breeding lines with translocations from T. timopheevii contain genetic loci responsible for resistance to spot blotch, fusarium and septoriosis (Ma and Hughes 1995; Christopher et al . 2007 ; Srinivasachary et al. 2008 ).
Diploid Wheats T. Monococcum (Am) and T. Boeoticum (Ab)
Stem rust resistance genes Sr21, Sr22, and Sr35 were transferred from diploid wheat T. monococcum to bread wheat (Kerber and Dyck 1973; Rouse and Jin 2011). Sr21 (Chen et al . 2015) and a number of other T. monococcum stem rust resistance genes different from Sr21, Sr22, and Sr35 (2 genes, Rouse and Jin 2011; gene SrTm4 , Briggs et al . 2015) confer resistance to highly virulent stem rust race Ug99.
Two powdery mildew resistance genes (PmTb7A.1 and PmTb7A.2) were identified and mapped on chromosome 7AL of another diploid wheat species , T. boeoticum (Chhuneja et al . 2012 , 2015 ) .
Aegilops Species for Wheat Improvement
Ae. Speltoides
Ae. speltoides, which is characterized by a high grain protein content along with fungal diseases resistance, was a donor of the leaf rust resistance genes Lr28, Lr35, Lr36, Lr47, and Lr51 (reviewed in Schneider et al. 2008 ; Todorovska et al. 2009 ). Among recent examples , genes encoding leaf rust resistance have been transferred from Ae. speltoides into T. aestivum (Adonina et al. 2012). Lr28, Lr36 and Lr47 genes were shown to be highly effective against leaf rust populations in most regions of the world, although, with the exception of the Lr28, remaining genes were not widely used in breeding practice for development of resistant wheat cultivars due to negative effects on agronomic traits.
Ae. speltoides is also a source of Sr32, Sr39, Sr47, and SrAes7t genes providing resistance of common and durum wheats to stem rust including race Ug99 (McIntosh et al. 1995; Faris et al . 2008 ; Klindworth et al. 2012 ; Yu et al. 2014) .
Two Ae. speltoides powdery mildew resistance genes (Pm12 and Pm32) were introgressed into common wheat chromosomes 6BL and 1BL respectively (McIntosh et al. 1995; Hsam et al. 2003). Pm12 is very effective against populations of powdery mildew pathogen worldwide. But this gene is not widely used in wheat breeding because of negative influence of alien chromatin on wheat productivity (Song et al . 2007 ) .
Recently gene Pm53 was located on the long arm of chromosome 5BL of winter wheat germplasm line and appears to be a new source of powdery mildew resistance that can be tracked with molecular markers in MAS schemes (Petersen et al. 2015) .
Ae. Tauschii
Ae. tauschii, the D genome donor of bread wheat has been used extensively for the transfer of agronomic important traits to wheat, including leaf rust resistance genes Lr41, Lr42, and Lr43 (Cox et al. 1994) as well as stem rust resistance genes Sr33 (1DS), Sr45 (1DS), and Sr46 (2DS) conferring resistance to highly virulent race Ug99 (Rouse and Jin 2011; Yu et al. 2015) . It was shown later that Lr40 is the same gene as Lr21, while Lr41 is a synonym of Lr39. Lr43 is not a unique gene because initial germplasm lines consist of the progenies with gene combination (Lr21 and Lr39) (McIntosh et al. 2013) .
Other two Ug99-effective stem rust resistance genes were recently transferred to bread wheat from chromosomes 6DS (SrTA10187) and 7DS (SrTA10171) of Ae. tauschii (Olson et al. 2013 ).
Ae. tauschii is often used for introgression of resistance genes into the genome of bread wheat through the development of synthetic hexaploid forms. Association mapping with the help of a set of synthetic hexaploid wheats revealed 2 novel stripe rust resistance loci on chromosomes 3DL and 6DS originating from Ae. tauschii (Zegeye et al. 2014). Stripe rust resistance genes were revealed on Ae. tauschii chromosomes 3DS (YrY206, Zhang et al. 2009) and 4DS ( YrAS2388 , Huang et al. 2011 ). Potential of this species for improvement of stripe rust resistance was also shown by Liu et al. (2013) .
Miranda et al. (2006, 2007) identified Ae. tauschii- derived wheat powdery mildew resistance genes Pm34 and Pm35 on wheat chromosome 5D . Sun et al. (2006) mapped 2 genes , PmY201 and PmY212, on chromosome 5DL of Ae. tauschii. Maxwell et al. (2012) characterized a novel Ae. tauschii-derived gene (MlNCD1) conferring resistance to powdery mildew , mapped to the short arm of chromosome 7D in more distal position compared to the previously known Pm38 gene.
Other Aegilops Species
Germplasm of the other Aegilops species (not related with hexaploid wheat origin) has been exploited to a limited extent for a search and transfer of the genes determining wheat resistance to fungal diseases. This is primarily due to methodological difficulties of introduction of foreign genetic material into the genome of common wheat by direct hybridization. Nevertheless, a number of genes for resistance to rust diseases was identified in the genomes of Ae. ventricosa (Lr37, Yr17, Sr38), Ae. geniculata (Lr57, Yr40, Sr53), Ae. triuncialis (Lr58), and Ae. peregrina (Lr59) (Seah et al. 2001; Kuraparthy et al. 2007a, b; Marais et al. 2008)
For translocation T5DL∙5DS-5MgS from Ae. geniculata, containing leaf and stripe rust resistance genes (Lr57, Yr40) the absence of negative effects on endosperm texture of winter wheat cultivars has been proven (Kuraparthy et al. 2009). Positive effects on bread-making quality was detected for translocation containing cluster Lr37-Yr17-Sr38 genes from Ae. ventricosa (Labuschagne et al. 2002).
A number of disease resistance genes have been transferred from other Aegilops species: Ae. umbellulata (LrU1, LrU2, YrU1), Ae. caudata (LrAC), Ae. variabilis (unknown gene), and Ae. variabilis (LrV, YrV) (Chhuneja et al . 2008; Riar Kaur et al. 2012; Spetsov et al. 2013). Apparent linkage drag was observed neither in the introgression lines obtained on the basis of Ae. umbellulata and Ae. variabilis, nor in their backcross progenies, suggesting that new genetic loci could be exploited commercially.
Rye as a Source of Disease Resistance Genes for Bread Wheat
Among the successful introduction of rye (Secale cereale L.) genetic material into the genome of common wheat only two translocations have practical value, and in both cases chromosome 1RS took part in these translocations.
The translocated 1RS chromosome arm of the rye cultivar ‘Kavkaz’ frequently occurs in wheat cultivars of European selection ( Villareal et al. 1998; Purnhauser et al. 2011). It confers disease resistance against powdery mildew (Pm8), stem rust (Sr31), leaf rust (Lr26) and stripe rust (Yr9) (Lukaszewski 2000). Cultivars with this so-called 1BL.1RS translocation (Mettin et al. 1973; Zeller 1973) showed high yield potential and multiple disease resistance (Rabinovich 1998; Kim et al. 2004 ; Belan et al . 2010 ).
Translocation 1AL.1RS, obtained on the basis of rye cultivar ‘Amigo’ contains genes for resistance to wheat aphid (Gb2), powdery mildew (Pm17) and stem rust (unknown gene). This translocation is spread mainly in the American wheat varieties. Translocation 1AL.1RS was also found to have positive effects on drought tolerance, grain protein content and yield (McIntosh et al. 1995; Kim et al. 2004).
Other wheat-rye translocations, such as T3AS-3RS with Sr27 gene, T4BS.4BL-5RL with Lr25, T6BS-6RL with Pm20, T2AS-2RS.2RL with Lr45, and T2BS-2RL containing the locus of resistance to Hessian fly are not widely used in breeding due to their negative effects on agronomic traits.
Conclusions and Prospects
Wild and cultivated wheat relatives and species from related genera are an inexhaustible source of genes providing resistance to diseases and insects. To date, more than 50 % of known genes determining resistance to rust diseases and powdery mildew originate from wheat relatives (McIntosh et al. 2013) . However, only a limited number of genes were utilized in practical breeding to improve genetic basis of bread wheat resistance. Others were used only for development of introgression and isogenic lines.
One of the main reasons for limited practical application of the resistance genes is the presence of alien genetic material tightly linked with the target gene and negatively influencing agronomic traits. For example gene Lr19 closely linked to the gene Y, determining the yellow color of flour is not used for development of resistance of wheat cultivars in those countries which traditionally prefer the flour of white color.
In recent years, the development of new molecular methods for tagging of disease resistance genes and technology of marker-assisted selection made it possible to eliminate excessive donor material, which may have negative effect on agronomic traits. In this way, for example, bread wheat lines with shorter introgression fragments containing Sr37 and Sr39 genes with effective resistance to stem rust were obtained (Yu et al . 2010; Zhang et al. 2012). The study demonstrated that the lines with reduced alien chromatin have no negative effects on productivity traits anymore.
Further difficulties can be related with insufficient level of alien gene expression due to divergence between bread wheat cis- or trans-regulatory elements and those of the donor species (Khlestkina et al. 2009; Shoeva et al. 2016) or suppression of alien genes by their orthologs in wheat (Hurni et al . 2014 ).
The recently developed approach for precise gene editing, CRISPR/Cas9 system (reviewed in Bortesi and Fischer 2015), has been already used successfully for editing resistance genes in wheat (Wang et al. 2014). This system allows making fine changes in plant genome and may help to overcome the difficulties mentioned above by editing regulatory sequences or direct insertion of desirable gene sequences without hybridization.
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Shumny, V., Khlestkina, E., Leonova, I., Salina, E. (2016). Broadening the Genetic Diversity of Bread Wheat Using Alien Germplasm: Emphasis on Disease Resistance. In: Korogodina, V., Mothersill, C., Inge-Vechtomov, S., Seymour, C. (eds) Genetics, Evolution and Radiation. Springer, Cham. https://doi.org/10.1007/978-3-319-48838-7_9
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