633.111:631.524.7

GENETIC CONTROL OF SEED DORMANCY AND PREHARVEST SPROUTING RESISTANCE IN WHEAT (review)

V.A. Krupnov, S.N. Sibikeev, O.V. Krupnova

The article discusses the allelism of Vp-1 gene in red-grained and white-grained genotypes and its meaning for resistance to preharvest sprouting. The diversity of resistance loci associated with pre-harvest sprouting, it mapping on the chromosomes, and also the environmental effects and genotype/environment interactions were analyzed. The possibility is shown to use molecular markers and alien genes in wheat breeding programs on resistance to preharvest sprouting.

Key words: seed dormancy, preharvest sprouting resistance, quantitative trait loci, molecular markers.

 

Wheat is one of three major food crops. When a bad weather occurs during the harvest season (frequent rains, dew, sharp fluctuations in air temperature), grain in the ear can germinate, which reduces its quality and yield (1, 2). Even the first signs of grain germination significantly reduce flour milling output, deteriorate dough physical properties - it becomes sticky, insufficiently flexible and provides the bakery of a very poor quality (3, 4). The white-grained varieties are the most affected by pre-harvest sprouting of grain (1, 5-9).

Germination usually correlates with activity of a-amylase (a-Amy-1),  which initiates starch to dissolve in the endosperm; three its genes-orthologues (a-Amy-A1, a-Amy-B1 a-Amy-D1) were identified and found to be localized in the long arms of 6th group of chromosomes (6AL, 6BL, 6DL) (10).

Seed dormancy. Seed germination begins after the completion of dormancy, which is associated with the gene Vp (Viviparous-1) first studied in maize (11). Vp- homologues (orthologues) were also found in other cereals (12). The synteny between Vp-1 genes has been established in wheat, barley, rice, wild oat (13-16). In the wild oat (Avena fatua L.), the gene AfVp-1 determines a much more profound and long-term seed dormancy than its orthologue in wheat (17).

In a soft wheat, three homologous genes Vp-A1, Vp-B1 and Vp-D1 (or TaVp-A1, TaVp-B1 and TaVp-D in the subgenomes A, B and D, respectively) (12 ) are localized in the long arm of 3rd group of chromosomes (3AL, 3BL, 3DL) at the distance of approximately 30 cM from Red-loci (13). In genotypes resistant to pre-harvest sprouting (eg, the Japanese variety Minamino), each of the Vp-1 genes operates as a transcription factor and plays an important role in determining seed dormancy, and their role is less significant in the varieties highly susceptible to pre-harvest sprouting. In the variety Minamino, the gene TaVp-B, on the one hand, activates the expression of Em gene controlling synthesis of a specific protein, on the other hand, it inhibits the expression of  a-amylase (18). It is believed that descending the role of Vp-1 genes in determination of seed dormancy could happen before the domestication of wheat as the result of mis-splicing in introns (12). A similar pecularity in the structure of Vp-1 has been also found in barley, rye, Brachypodium pinnatum, Agropyron repens, Elymus repens and Thinopyrum scripeum (19).

The interactions between seed embryo, endosperm and aleurone are significantly affected by the regulatory proteins thioredoxines produced by the gene(s) Trxs, as it has been demonstrated on transgenic plants of barley and wheat (20-22). In wheat lines with reduced expression of Trx, pre-harvest sprouting in a greenhouse or in field conditions is considerably delayed without diminishment of final harvest (21).

The role of seed integument is not enough investigated, although it has been long ago established the connection of seed dormancy with Red-alleles; it has been reported that Red-alleles are localized in 3AL, 3BL, 3DL and determine red coloration of seed (23, 24). The replacement of Red-allele(s) with recessive alleles or removal of a seed husk are accompanied with the significant decrease in seed dormancy properties (24). In sets of white-grained genotypes (all Red-alleles are in recessive state), the variation in this characteristic is commonly much wider than in red-grained sets (8, 9). The contribution in seed dormancy of each Red-allele is usually small and hard to define (23). The red-grained genotypes susceptible to pre-harvest sprouting are also known to exist (6). The connection of seed dormancy with grain coloration has been also established in wild rice (25, 26) and Arabidopsis (27-29). The basics for this connection are not entirely clear (the pleiotropy effect of Red-genes, or linking to other genes), as well as the role of a seedcoat in seed dormancy and resistance to pre-harvest sprouting in respect to white-grained genotypes (30). It is possible that in seedcoat, some other genes are expressed to determine seed dormancy in addition to Red-genes (26, 31, 32).

Resistance to pre-harvest sprouting. Resistance is a complex phenomenon caused by the effect of Vp-1 genes providing seed dormancy, on the one hand, and by a number of other mechanisms and the expression of other determinants – on the other hand (33). The level of resistance to pre-harvest sprouting can be affected by gibberellins-insensitive Rht-loci (34), ear morphology (35, 36), waxy film on ear glumes (37), the content of germination inhibitors in spikelets base (38-41), florets openness, fitting of flower bracts, the presence of ear awns, an angle of ear bending, plants lodging and many other characteristics (8, 9, 39, 42-46).

There are two key hormones affecting the regulation of seed dormancy and germination - abscisic acid (ABA), and gibberellins (D). ABA is the main signal factor for embryogenesis, the start of seed dormancy and its maintenance (47, 48). In the first half of seed maturation, ABA content in seeds grows, and later it gradually reduces with dehydratation of seeds (49). In Arabidopsis thaliana and Nicotiana tabacum, the initial increase of ABA content is associated with maternal tissue, but the own ABA synthesis by embryo begins from the middle of seed ripening phase. The studies of reciprocal hybrids suggest the influence of maternal ABA on the induction of seed dormancy.

Gibberellins contradict ABA by inducing the activity of a-Amy-1.  Upon the mutant Arabidopsis thaliana, the importance of gibberellins in endosperm destruction has been demonstrated, as well as their role in providing of the embryonic growth potential necessary for penetration through a seedcoat to soil surface. Gibberellins induce the activity of  a-Amy-1 (50), while ABA, apparently, prevents a-amylase expression and the programmed cell death in aleurone (51). Mechanisms of ABA-sensitivity in seeds were studied mainly in A. thaliana (47). The six genes ABI (ABA-insensitivity) and two gene ERA (enhancing the response to ABA) have been revealed in mutants of this crop. These genes operate in seeds as a part of ABA-signal transduction system, playing the important role in determining seed dormancy (47). The in silico analysis of soft wheat diploid progenitors (Triticum monococcum L. and T. boeoticum Boiss) helped to identify the homologues for ABA-signaling genes of Arabidopsis (15). The content of ABA and gibberellins, as well as their balance in seeds are the important controlling factors in seed development, maturation and germination. However, the ways of regulation of ABA- and gibberellins-signaling by TaVp-1 aren’t unclear yet (18).

Germination depends not only on the antagonism between ABA and gibberellins, but also on temperature, water regime, nutrients content and supply, oxygen and other external factors (47, 52). The main role in pre-harvest sprouting resistance belongs to specific genes found in the loci QPhsR (Quantitative Pre-harvest Sprouting Resistance) (10). The loci vary in degree (strength) of their influence on the resistance: some provide the major effect (major QTL), others - minor (minor QTL). The first group includes the loci, which determine more than 10% phenotypic variability of a certain determinant, the second group - less than 10% (53-55).

In wheat, for mapping and identification of QTL / QphsR loci, there are four typically used methods of assessing phenotypes: germination of threshed seeds under laboratory conditions (germination index), germination of grains in the ear, measuring the Hagberg falling number and determination the activity of a-amylase (36, 55-59). The combination of these methods for evaluation of phenotypic resistance to pre-harvest sprouting and genome molecular analysis reveal new opportunities for QphsR identification and mapping. The table shows the results of pooling the data of available publications about identification and localization of QphsR and Vp-1 in chromosomes of soft and hard wheat (without specifying the names of these loci and their associated flanking molecular markers).

Wheat chromosomes containing alleles of the gene Vp-1 and QTL/QphsR loci
determining pre-harvest sprouting resistance of grain

Genotype / population

Chromosome, gene, allele, locus

Reference, number

Hexaploides

Red-grained genotypes

Renan/Récital

3AL, 3BL, 3DL, (Red and TaVp-1), 5AL

29

Récital

Vp-1Bb

60

Altria

Vp-1Bb

60

AC Domain/Haruyutaka

4AL, 4BL, 4DL

53

Boxer/Soleil

4BS

61

N72.72

3DL, QTL from Triticum sphaerococcum

62

RL4137/Timgalen

1BS, 4BS, 4BL

61

Zen/CS

2AL, 2DL, 3AL, 3BL, 7DL

54

Zen

3AS, (3AL, Vp-1)

63

CS

6AL

54

Zen/CS

3AS, 4AL, 4BL

64

Halberd

7BL

57

Halberd

3BS, 7BL

65

ITMIpopulation

2B, 3B, 3B, 3D, 5D, 6A

66

ITMIpopulation

3AS, 4AL

67

SW95-50213

4AL

57

SW95-50213/Cunningham

4AL

68

AC Domain

4A, 3D, 5D

69

RL4452/AC Domain

3A, 4A, 4B, 3D, 7D

70

Minamino

TaVp-B1 (correct splising in 3rd intron)

18

Red – and white-grained genotypes

SPR8198Red/HD2329w

6B, 7DL

71

SPR8198/HD2329

3AL (linked with Red-gene)

56

SPR8198/HD2329

1A, 2AL, 2AS, 2B, 2DL, 3AL, 4B, 7A, 3BL

72

Kitamoe/Munstertaler

4AL

73

Spica/Zen

3AS, 4AL

74

Syn37/2*Janz

1DL, 2DL, 3DL, 4AL

58

AC Domain/White-RL4137

3AS, 2A, 3D, 5DS (total 2 QTL)

69

OS21-5/Haruyokoi

4AL

75

PH132k/WL711 amb, India

11 QTL, including M-QTL on 6AL

76

Red-RL4137

4AL, 3D

77

Forno/Oberkulmer (no data on grain coloration)

2AL, 1BS, 3AS, 3BL, 4D, 5AL, 5AS, 5AL, 6D, 7BL (total 13 QTL)

36

White-grained genotypes

Yongchuanbaimai

3BL, Vp-1Bb, insert in intron 

4

Xinong 979

3BL, Vp-1Be, deletion in intron 

4

NY18/NY10

3BL, 4AL, 5DL, 6BL

78

Cranbrook/Halberd

2AL, 4AL, 2DL

62

Clark Cream

2BL

79

AUS1408

3DL, 4AL

62, 57

AUS1408 (Red)

4AL, 5AL

80

SUN325B, Australia

3BL, independent from Red-gene

30

QT7475/Sunco

4AL, M-QTL

30

SUN325B/QT7475

(4AL, M-QTL), 3BL, (3DL, m-QTL)

30

White-RL4137

3D

59

Janz × AUS1408

4AL, M-QTL

68

CN19055 (red)

4AS

55

CN19055/Annuelo

4AS, 4AL

55

Rio Blanco/NW97S186

(3AS, M-QTL and m-QTL), 2BL (2B.1 and 2B.2, both m-QTLs)

81

Cayuga/Caledonia, USA

(2B.1, M-QTL), 2D.1, 3D.1, 6D.1 (total 15 QTLs)

82

CS/Aegilops tauschii

6DL

67

Syn36, Triticum durum/Ae. tauschii

3D, 4A

77

Diploid genotypes

T. monococcum/T. boeoticum

3Am, 5Am

15

Tetraploid genotypes

CI13102/Kyle

1A,M-QTL

83

Altar84 (T. durum)

4A, (4A.1, 4A.2)

58

According to publications data (see Table.), there are more than 130 QTL / QphsR loci identified and mapped in the chromosomes of different wheat genotypes. Some of them may be identical, i.e. the total number of non-identical loci is, apparently, much smaller. In most cases, QphsR is located in the long arm of chromosome, as reported by many researches (29, 53, 55, 61, 63, 64, 66, 81). The highest frequency of QTL occurrence was detected in the chromosomes 3A, 3B, 3D, the second - 4A, 4B, 4D, the third - 2A, 2B and 2D (55, 62, 72, 78, 84, 85).

Chromosomes of the 3rd group of homeologues. In this group, there are 54 QphsR loci, including 18 loci in 3A, 15 – in 3B and 17 - in 3D chromosome. In all these cases except one, QphsR are localized in the long arm of chromosomes. Obviously, such concentration and position of QphsR aren’t accidental - as it was already noted, Vp-1 homologues and Red-genes are located in this region. It is possible that in some cases Vp-1 performs the functions of QphsR (4, 19, 86).

Multiplicity of Vp-1 alleles B. Using STS-marker for Vp-1B3 has allowed to distinguish the alleles of Vp-1B gene - particularly, the alleles Vp-1Ba, Vp-1Bb, Vp-1Bs, and Vp-1Bd (4, 87), which provide significantly different contribution in seed dormancy and pre-harvest sprouting. In contrast to a genotype containing Vp-1Ba, genotypes containing Vp-1Bb and Vp-1Bc have insertions or deletions in the 3rd intron (4). In the resistant to pre-harvest sprouting variety Yongchuanbaimai (Vp-1Bb, germination index 0,14), embryo is more sensitive to ABA than the susceptible variety Zhongyou 9507 (Vp-1Ba, germination index 0,84). The authors believe (4) that the insertion or deletion in the 3rd intron might affect the expression of Vp-1B, transcripts’ accumulation and gene sensitivity to ABA, thus influencing seed dormancy and resistance to pre-harvest sprouting in wheat grain ( 4). The close correlation between transcripts accumulation and the level of resistance to pre-harvest sprouting was previously established in other wheat varieties (86).

The study of 490 wheat varieties widespread in Europe (87) has revealed ranking Vp alleles by frequencies of their occurrence: Vp-1Ba (54%) > Vp-1Bc (21%) > Vp-1Bd (20%) > Vp-1Ba + c ( 4%) > Vp-1Bb (1%). Interestingly, that in the UK varieties, the frequency of Vp-1Ba occurrence was 76%, while in Sweden - only 19% (87), and there’s no data on what caused this distribution.

We have already highlighted the close association of QTL/QphsR with Red-genes in certain genotypes (29, 69, 88). A direct relationship between the resistance to pre-harvest sprouting and grain coloration as a marker was demonstrated by many researchers (1, 23, 56, 66, 89, 90). However, as already noted, the molecular basics for this phenomenon are not entirely clear (4, 91). The method of molecular markers can reveal new opportunities for studying the quantifying effect of Red-alleles in the control of resistance to pre-harvest sprouting (4, 92).

In short arms of the 3rd  group of homoeologues, QphsR can be found infrequently, and some of them are major (54, 63, 64). Thus, the 3AS chromosome of the red-grained Japanese variety Zen contains the locus QPhs.ocs-3A.1  providing 23-38% of phenotypic variation in seed dormancy; authors suggest, that it operates independent from TaVp-1 or Red-A1 loci.  Meanwhile, QPhs.ocs-3A.2 localized in the long arm of 3A chromosome causes a minor effect (63). Interestingly, that in the white-grained variety Rio Blanco, the major QTL QPhs.pseru-3AS providing over 41% total phenotypic variation in pre-harvest sprouting resistance (data of three greenhouse experiments), was also identified in 3AS (81); it is unknown how much these loci differ in these two varieties. In the USA, the variety Rio Blanco is used in breeding wheat for resistance to pre-harvest sprouting. (81, 93-95).

In T. monococcum, the long arm of 3Am chromosome contains two minor QTLs, each of which provides about 10% variation in seed dormancy; both these genes are considered to be probably responsible for resistance to pre-harvest sprouting in wheat (15).

Chromosomes of the 4th group of homeologues This group includes the second highest number of identified major and minor QphsR loci. The major QphsR locus localized in 4AL was found in both white- and red-grained genotypes of various origins (29, 53, 57, 63, 64, 66, 67, 73, 78, 88, 96, and 97). In the population of recombinant inbred lines (RIL) obtained by crossing Totoumai A / Siyang 936,  M-QTL was identified in the chromosome 4AL; this gene determines 28% variation in seed dormancy and 31% resistance to pre-harvest sprouting in China (81).

Using tests with sets of microsatellite markers flanking QPhsR in soft wheat the 3rd , 4th , 5th  and 6th groups of chromosomes, the four types (clusters) of gene alleles were identified in 4AL: Red-RL4137, White- RL4137, Aus1408 and Syn36 and Syn37, which, apparently, in combination with other genes determine different resistance to pre-harvest sprouting and seed dormancy (55, 59, 77).

The type Red-RL4137 (red grain). This line, except the key locus QphsR in the chromosome 4AL, has QphsR locus in 3D (77). Stability of this type is widespread in Canada, where its sources are used in breeding of both red- and white-grained varieties (77, 98). Meanwhile, the white-grained line White-RL4137 (Red-RL4137 * 6 // Tc/Poso48) - analog of the line Red-RL4137 – demonstrates the degree of resistance to pre-harvest sprouting approaching the red-grained recipient. The progeny from the cross AC Domain (red grain) / White-RL4137 (white grain) was found to contain the 11 identified QPhsR loci not associated with red color, four of which are located in the chromosomes 3A, 3B and 3D, and one – in 5D (69).

The type Aus1408. AUS1408 (white grain) is a local variety from South Africa. This genotype is used as a donor of resistance to pre-harvest sprouting in selection of white-grained varieties in Australia, China and several other countries.

The line Kenya321 (white grain) - a derivative from the cross Australia45C5 / / Marquis/Aguilera8; this line demonstrates the level of resistance to pre-harvest sprouting equal to Aus1408, while its mechanism is, probably, different from previous models of resistance determined by one or more genes (59).

The types Syn36 and Syn37. Differ from previous by the presence of heterogeneous genes for resistance to pre-harvest sprouting. The line Syn36 was selected from the combination Altar84/18905 (sample T. Tauschii = Ae. Tauschii = Ae. Squarrosa L.), Syn37 – from the combination Altar84/18836 (sample Ae. Tauschii) (59). Syn36 has the higher degree of resistance to pre-harvest sprouting is significantly than  Syn37 (microsatellite analysis showed differences between the lines by QPhsR in 3DL) (77). QPhsR from Syn36 and Syn37 haven’t been introduced into new varieties yet.

QphsR localized in the long arm of the chromosome 4Am in T. monococcum  provides a significant influence on seed dormancy (15). This locus may correspond to the main QTL in the soft wheat 4AL, which had been previously identified by two groups of researchers (57, 73), and it seem to be homoeologeous to QTL in the barley 5HL (68). The 4th group of homoeologeous contains gibberellins-insensitive Rht-loci that may affect the resistance to pre-harvest sprouting (34). Two of them (Rht-B1b and Rht-B1c) are localized in the chromosome 4BS, Rht-D1b - in 4DS (10), but QTL/ QphsR wasn’t identified on these arms of chromosomes in the studied genotypes.

Chromosomes of the 2nd group of homeologues. In the short arms of 2A, 2B and 2D, there are three identified genes (TaAFPs) involved in regulation of ABA-signaling - TaAFP-A, TaAFP-B and TaAFP-D, respectively (85). The genes-orthologues were also identified there - Ppd-B1 (in the chromosome 2BS) and Ppd-D1 (in 2DS), which control the reaction to photoperiod. However, QphsRs are extremely rare and usually minor (36, 54, 62, 66, 78). Two QPhsR loci - in 2AL (major) and in 2BL (minor) - were identified in the RIL population from the cross SPR8198 (red grains) / HD2329 (white grain) (72). The role of these genes as donors in breeding for resistance to pre-harvest sprouting is not known; it is suggested, that, for example, in the white-grained variety Rio Blanco, the minor loci (QPhs.pseru-2B.1 and QPhs.pseru-2B.2) can be involved in breeding programs using molecular markers (81).

Chromosomes of the 1st group of homeologues. Some populations are known to possess QPhsRslocalized in the chromosome 1A (36, 66, 72, 78, 83). Thus, one locus (QPhs.ccsu-1A.1) was identified in the short arm of 1A in the RIL population from the cross SPR8198 with HD2329 1A (72).

Chromosomes of the 5th group of homeologues. Using the methods of measuring falling number and  α-amylase activity (36), QPhsR was identified in the chromosome 5A and found to be responsible for 49,7% of phenotypic variation in the first characteristic and 38,5% - in the second one. These QTLs significantly interact with environmental factors, as well as in the population of ITMIpop lines, whose 5D also contains QPhsR (66). In the RIL population obtained by the cross AC Domain (red grains) / White-RL4137 (white grain), 5D contains the identified locus QSi.crc-5D, which is also highly sensitive to external influences (69). In T. monococcum, the major QPhsR  localized in the long arm of 5Am determines 20-25% variation in seed dormancy (15).

Chromosomes of the 6th group of homeologues. There’s a little data  about QPhsR identification and localization in this group of chromosomes (36, 66, 71, 76, 78, 82).

Transgressions. Transgressions have been observed in populations of interspecific hybrids (23, 66, 64), as well as in the hybrid progeny from crosses of wheat with khorasan (36). In the population obtained by the cross AC Domain/White-RL4137, the line more resistant to pre-harvest sprouting than the resistant variety AC Domain was revealed, while the others appeared to be more susceptible than the sensitive variety White-RL4137 (69). The interesting fact has been observed in the white-grained line CN19055 selected from the combination AUS1408/RL4137: this line performed the higher degree of resistance to pre-harvest sprouting than its parents. Microsatellite haplotype analysis of the line CN19055 revealed the presence of QPhsR from AUS1408 (in 3D) and another QPhsR from RL4137 (in 4A) (77).

Environmental effects. In a field experiment, the raising number of uncontrollable external factors complicate the evaluation of QPhsR manifestation compared with greenhouse conditions. It has been shown, for example, that phenotypic variation in resistance to pre-harvest sprouting provided by QPhs.pseru-3AS locus, was significantly less in the field experiment than in a greenhouse (81); according to the authors, this fact contributes to more reliable identification of QphsR, especially with minor effect (81). Some genotypes are more sensitive to the environment. For example, the medium-tolerant to pre-harvest sprouting genotypes AC Karma, HY476 and CFR8-12 (New Zealand) in some countries are characterized as tolerant, in others - as sensitive (52, 59, 66, 98-100).

Loci interactions. Along with an additive interaction, the epistasis, as well as interaction of QPhsR with external environment have been established (for germination index and germination of grains in the ear) (58). Both additive and epistatic effects raise phenotypic variance of resistance to pre-harvest sprouting, which indicates the opportunity for breeding of this characteristic. It is possible, that hexaploid wheat hybrids will manifest the expression / suppression of pre-harvest sprouting resistance, similarly with the resistance to rust pathogens - for example, the response to Puccinia striiformis f. sp. tritici (101, 102). Thus, the high sensitivity to pre-harvest sprouting of the variety Janz was found to be associated with the presence in D-subgenome of suppressor genes for this determinant, which is absent in the synthetic hexaploid (58). In the genotype of spring wheat, 6Agi (6D)-chromosome from Agropyron intermedium Host. is known to provide the high resistance to leaf rust caused by P. recondita Rob. ex Desm. (F) sp. tritici (103), but all the lines created using this chromosome were found to reveal a trend of decreasing resistance to pre-harvest sprouting (104).

Heterogeneous genes. The highly-effective genes controlling seed dormancy have been found in several samples of Ae. tauschii (40). Some of these samples contained in glumes the unknown inhibitors suppressing water transfer to seeds, which increases their resistance to pre-harvest sprouting in addition to QPhsR loci effects (40).

In the progeny  from crossing the diploid species T. monococcum L. (Tm) and T. boeoticum Boiss (Tb), four homoeologues (TmVp-1, TmABF, TmABI8 and TmERA1) have been identified in the chromosome 3Am and one (TmERA3) - near the centromere in the long arm of 5Am (15). The two-year study in controlled conditions allowed to identify one major QphsR in the long arm of 5Am, two minor QTLs  in the long arm of 3Am and one minor QTL in the long arm of 4Am. The QphsR in 5Am determines 20-27% of phenotypic variation, while with each of the three other QphsRs - approximately 10%. The QTL identified in 5Am can be the orthologue for the QTL in wheat 5A, and the QTL in 4Am - for the main QTL in 4AL, as it was reported previously (57, 73). It is assumed that TmABF and TmABI8 may be the candidate genes for resistance to pre-harvest sprouting (15).

Wheat plants possessing transgenic Vp-1 from Avena fatua were found to be more resistant to pre-harvest sprouting than control genotypes (12).

Markers. The confident distinguishing of phenotypes resistant and non-resistant to pre-harvest sprouting is considered to be one of the conditions for reliable identification and localization of QPhsR (36, 55-59, 105). When phenotyping crops, it should be considered that the indicators of falling number and a-amylase activity rather reflect destructive changes in endosperm than sprouting (PHS – pre-harvest sprouting per se) (66, 72). However, it’s very important to know that high activity of a-amylase isn’t always associated with presence of genes / loci for resistance to pre-harvest sprouting, but this can be the result of defective genes providing activation of a-amylase prior to seed dormancy (i.e. in a process of development) without apparent symptoms of germination. This phenomenon is known as prematurity a-amylase (PMAA), or late maturity a-amylase (LMA) (88, 106), which is accompanied by a sharp decrease in falling number of grain and deterioration of bread baking qualities. It has been suggested that the precocious a-amylase synthesis is controlled by one or two recessive genes or loci in the chromosomes 3B and 7B (106) and is usually induced by thermal shock (cold or heat) on the 25th – 30th days after flowering (106). It has been shown, that cold affects enzyme synthesis more than heat (107). Premature a-amylase synthesis has been also observed in barley, rye (105), triticale (106). Therefore, one of the conditions for mapping the QPhsR loci should be the preliminary excluding from study the  genotypes with defective genes PMAA or LMA. It should be also considered that the expression of QPhsR can be affected by genes controlling morphological and other determinants (for example, gibberellins-insensitive Rht-loci, see above). Consequently, applying of indirect methods for genotype phenotyping  (determination of falling number and a-amylase activity) it is necessary to complement them with determination of seed germination index and / or germination of grains in the ear. By the way, the method of laboratory seed germination is thought to be the most rapid and inexpensive one, allowing to assess the resistance of grain to pre-harvest sprouting not only in wheat, but also in barley (108).

The efficiency of traditional selection from early hybrids generations under the appropriate phenotype is very low for several reasons. Firstly, the field conditions are not always favorable. Secondly, the determinant expression is significantly affected by environmental factors, as well as by the interaction between QPhsR and environment (43, 46, 53, 58, 74, 78, 107, 109-112). The comparative study of the red- and white-grained lines BC1F7 grown in a greenhouse and in field has proved the significant influence of cultivation environment on germination index (the white-grained genotypes manifested the most contrasting responses) (112). Drought and high temperatures in period of grain formation and ripening enhance dormancy genes expression, which should be considered when screening genotypes by their resistance to pre-harvest sprouting (46). Thirdly, the difficulties of large-scale selection of grains / ears for the analysis of resistance to pre-harvest sprouting may cause non-simultaneous reaching of physiological maturity by grains from different genotypes. In most cases, selection is based on visual assessment of leaf, culms and spikelet glumes (loss of green color) (55, 59, 112). The method of molecular markers gives an opportunity for creation the controlled combination of different QPhsR in one genotype (building QTL “gene pyramids”). It is of particular interest to use molecular markers in breeding of white-grained varieties possessing inactive QPhsR linked with Red-genes, which significantly restricts the variety of donors compared with breeding of red-grained forms.

So, over the last decade, quite a lot has been achieved in understanding of processes providing seed dormancy and resistance to pre-harvest sprouting. The multiple alleles of the gene Vp-1 in both red- and white-grained wheat genotypes have been established, and their effects on resistance to pre-harvest sprouting were shown. The major and minor QPhsR loci have been identified and localized in chromosomes; the genetic diversity has been studied in germplasm of bread wheat and relative crops. The molecular markers for many QPhsR have been identified, and the effects of interaction between QPhsR and external environment were studied. The effectiveness of using the molecular markers for building genes / loci pyramids of resistance to pre-harvest sprouting has been proved, and the possibility of genetically engineering approach to solving this problem was shown. However, the molecular mechanisms of QPhsR expression, their interactions among themselves and with other genes, as well as transcription factors and environmental conditions are far from solved. It’s necessary to further improve the methods of selection for increased resistance to pre-harvest sprouting, which should be completed by solving the problems of varieties adaptation to climate fluctuations, obtaining stable yields and grain quality.

The authors are grateful to Doctor of Biological Sciences, Professor V.A. Poukhalskii for his valuable comments and suggestions on improvement of the manuscript.

 

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South-East Science and Development Institute  of Agriculture, Russian Academy of Sciences,  Saratov 410010, Russia
e-mail: vasiliy_krupnov@mail.ru

Received
November 24, 2009

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