Variability of breeding system, caryopsis microstructure and germination in annual and perennial species of the genus Brachypodium P. Beauv.
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The basis of any patterns of variation in plant populations is the breeding system they express. In the genus Brachypodium, the breeding system ranges from autogamy in facultatively chasmogamic Brachypodium distachyon to allogamy in obligatory chasmogamic B. pinnatum. B. distachyon and B. sylvaticum appeared to be extremes with respect to dormancy and germination behaviour. Winter and facultatively biennial forms of the annual B. distachyon expressed an intermediate dormancy behaviour towards perennial species. Perennial species such as B. pinnatum, B. phoenicoides, B. rupestre and B. sylvaticum demonstrated allogamic behaviour and were highly dormant. The storage potential of hemicelluloses in endosperm cell walls and suberin-phenolic synthesis in testa and pigment strand differ distinctly between annuals and perennials. The suberized glumellae base and caryopsis attachment restrict the growth of coleorhiza and can change growth relationships between root and coleoptile. Coleorhizal hairs facilitating water capillary adhesion to an embryo are developed in both types of Brachypodium species, but in perennial types they are less efficient. The pattern of development of coleorhizal hairs distinguishes Brachypodium species from members of the tribe Triticeae. The coleorhizal hairs are less developed in Triticeae. This trait is variable at the populational level, especially in heterozygous populations (B. phoenicoides). Both extremes in terms of dormancy, i.e. B. distachyon and B. sylvaticum, revealed inter- and intrapopulational variability of germination.
KeywordsAnnuals Brachypodium Breeding system Dormancy Germination Perennials Seed structure
The panmictic status of heterozygotes in a population with randomly exchanged genes is rarely found in nature. Deviations from panmixis are caused by the small size of populations, their non-random distribution and isolation. A deficiency in heterozygotes can be caused by self-pollination of chasmogamic flowers (Richards 1986). Populations of Brachypodium Beauv. species are good examples of non-random frequencies of genotypes and phenotypes. A reduction in the frequency of heterozygotes may be realized in Brachypodium via autogamy or geitonogamy. This may occur in B. distachyon (L.) Beauv. and B. sylvaticum (Huds.) Beauv., which express high levels of self-compatibility (Khan and Stace 1999). In populations of perennials a degree of equilibrium between generative and vegetative reproduction has been noted, for instance in Brachypodium pinnatum (L.) Beauv. (Schläpfer and Fischer 1998). Kłyk (2005) reported a high level of diversity in terms of the generative offer in the genus Brachypodium. This offer is larger in perennials and smaller in B. distachyon; however, in the latter species chasmogamy, due to lodiculae activity, is common (Kosina and Pietrzak 2011; Kosina and Tomaszewska 2012). Sanders and Hamrick (1980) pointed out the importance of interaction between variation in breeding system and environment. They evidenced that in a self-fertilizing perennial, Elymus canadensis L., outcrossing is widely variable among populations. For pairs of autogamic grasses from the genera Avena L. and Bromus Scop., Jain (1979) proved that heterozygosity is higher in Avena barbata Pott ex Link and Bromus rubens L. than in A. fatua L., and B. mollis L. In these grasses, the rate of outcrossing is as high as several percent, but in Festuca microstachys Nutt., probably a cleistogamic species, it is 0 % (Grant 1981). Allen and Meyer (2002) proved that interpopulational variation of germination traits in Bromus tectorum L. exceeds 90 %. The breeding system of this grass is very close to that in B. distachyon.
In all perennial species of Brachypodium the anthers are remarkably extrorse, while in B. distachyon they are so in suitable weather conditions. In addition to dormancy and germination, variation in breeding system is the basis of the variation of all the features of any organism. Baskin and Baskin (2004) classified plants into the following five types of dormancy: physiological, morphological, morphophysiological, physical and combinational. The morphophysiological dormancy has been recognised as an ancestral state of seed plants and physiological dormancy as the most common (Willis et al. 2014). Seeds of annual cereals exhibit physiological dormancy. Naked grains, compared to hulled ones, have shorter dormancy (Grzesiuk and Kulka 1988). The situation is the same in the annual Brachypodium distachyon. The perennials of the genus Brachypodium seem to be different. However, before finding any answer, the most important factor is Baskin and Baskin’s statement (Baskin and Baskin 2004) that dormancy is a typical quantitative multigenic characteristic expressed under the significant influence of environment.
The following review complements the data on relationships between variability of diaspore microstructure and dormancy-germination in various species of Brachypodium using original research results. Some comparisons to the members of the tribe Triticeae L. are also provided.
A note on materials and methods
annual: B. distachyon (Bd, different accessions were numbered or marked by short symbols for the origin country),
perennials: B. pinnatum (Bp), B. phoenicoides (L.) Roem. et Schult. (Bph), B. rupestre (Host) Roem. et Schult. (Br), B. sylvaticum (Bs) with additional markings such as for B. distachyon.
Among species of Brachypodium, only B. pinnatum has been used for breeding purposes (K. Hammer, pers. comm.).
Some references and comparisons were made to certain members of the tribe Triticeae, such as wheat, rye, goat-grass and amphiploids.
All the studied material, regardless of whether it was analysed in field plots or in Petri dishes, was tested under equal environmental conditions according to an experimental design in the form of the one-way classification of a completely randomized set, for small samples (n = 30). The breeding system was evaluated using several characters of anthers and pollen grains, as had previously been done by McKone (1985, 1987), Hammer (1987, 1990) and Kłyk (2005). Dormancy was tested in terms of the percentage of germination of diaspores and root growth rate at daily intervals. The details of microstructure were studied on caryopsis cross-sections or germinating diaspores under various microscopes: stereo-, Amplival polarizing (Carl Zeiss Jena) and an Olympus BX60 epifluorescence. Numerical analyses of multivariate data for operational taxonomic units (OTUs, accessions, species) were executed with the application of the non-metric multidimensional scaling method, nmMDS (Rohlf 1994) and according to Kruskal’s proposal (Kruskal 1964). OTUs were plotted in a 3D-minimum-length spanning tree (MST) according to Rohlf’s proposal (Rohlf 1981).
Variation in the Brachypodium breeding system
Studies conducted by Kłyk (2005) evidenced that the breeding system of Brachypodium is variable within a broad range. Two extreme types of anther structure were described in Brachypodium (Kosina and Kłyk 2011; Kosina and Tomaszewska 2012). The first, displaying short anthers with few large pollen grains, is typical for the autogamic species, B. distachyon. The second one has long anthers with many small grains and is noted in allogamic species, e.g. B. pinnatum. A total of 271–582 pollen grains were developed in the anther of B. distachyon, while in B. pinnatum, a fully allogamic species, this range is between 5000 and 7640 grains. The highest developmental correlation (r = 0.93, significant for α = 0.001) exists between the length of anther and the number of pollen grains developed in it. Other examples of similar range of variation were discovered between annual autogamic versus perennial allogamic Hordeum vulgare L. and H. bulbosum L. (Hammer 1976), Secale sylvestre Host and Secale cereale L. subsp. afghanicum (Vav.) Hammer, comb. nov. (Hammer et al. 1987), and between Bromus tectorum and Bromus inermis Leyss. (McKone 1989). In bromegrasses, the interplant variation was low in autogamic B. tectorum and high in allogamic B. inermis. The above mentioned developmental correlation evidences that pollen mother cells are arranged in one cell layer in anther sacs and any increase of the pollen grain number can be achieved by increasing the length of anther. Such a structure of grass anther sacs was presented by Bhandari (1984) and Batygina (1987). However, this pattern of anther development can be changed in grass hybrids or mutants. For instance, in an intermediate form between Avena sterilis subsp. sterilis L. and A. sterilis L. subsp. ludoviciana (Durieu) Gillet et Magne, numerous large pollen grains were formed in the long anthers (Kosina 2015).
All the species of Brachypodium express chasmogamy and this shows the possibility of intra- and interspecific hybridisation within the genus. Chasmogamy is very clear in all Brachypodium perennials. In B. distachyon, all the studied ecotypes are chasmogamic under moderate humidity and temperature (Kosina and Tomaszewska 2012). Vogel et al. (2009) suggest that polyploid ecotypes of B. distachyon are more chasmogamic than diploid ones in a greenhouse, but this is not confirmed in our collection under field conditions. Artificial hybrids between perennial highly chasmogamic species of Brachypodium have been obtained and have shown good fertility, but no seeds have been developed in hybrid plants between B. distachyon and related perennials (Khan and Stace 1999). Our last data prove that even spontaneous interspecific hybridization, including B. distachyon as a mother plant, is possible; however, a hybrid plant expressed complete (100 %) pollen grain sterility. Brachypodium phoenicoides was considered here to be a pollen donor (Kosina and Tomaszewska 2014b). Such a level of pollen sterility would not be possible after an intraspecific cross-pollination.
Auto-allogamy intervariability, chasmogamy versus cleistogamy, with many intermediate types between the extremes, was exemplified in many grasses. In bromegrasses, the anther length and total volume of pollen grains per anther have wide interplant variation in allogamic Bromus inermis, an intermediate range of variation in B. kalmii A. Gray, B. ciliatus L. and B. latiglumis (Shear) Hitchc. which expressed a moderate level of outcrossing and a narrow range of variation in a facultative obligatory selfer, B. tectorum (McKone 1987, 1989). Intraspecific variation of some characteristics of breeding system is well exemplified in cereals by intercultivar differences. The level of chasmogamy presented as the number of extrorsed anthers from the flower ranges from 1.42 to 2.88 among winter common wheat cultivars (Keydel 1972). The length of anther, being a good indicator of pollen grains quantity, ranges from 2.93 to 3.20 among cultivars of Hordeum vulgare (Hammer 1975). However, a successful pollination and seed setting can also depend on many environmental factors. For instance, irrigation caused a shift from chasmogamy to cleistogamy in B. rigidus Roth and B. diandrus Roth (Kon and Blacklow 1990). Such variability was also created seasonally and appeared even within a single inflorescence in B. carinatus Hook. et Arn. Stress conditions such as higher temperature and lower moisture or autumn weather induced cleistogamy in this bromegrass (Harlan 1945). The morning and afternoon temperatures and air humidity appeared to be the most favourable for chasmogamic flowering of many grasses (Kevan and Tikhmenev 1996).
Thus, the level of heterozygosity in populations of Brachypodium will be high in allogamic B. pinnatum and species close to it, and proportionally lower in autogamic B. distachyon. This heterozygosity versus homozygosity, interacting with environment, will determine the patterns of all the variation in populations, including diaspore microstructures and levels of dormancy and germination dynamics. Andersson and Milberg (1998) studied variation in seed dormancy for three weed species belonging to three genera. They analysed dormancy between individual plants, between populations and between years; however, no mention was made of the breeding systems of these taxa. Therefore, their conclusions are seriously biased as a result of the lack of such information.
The above data show that in wild grasses, including Brachypodium, their life form seems to be correlated with breeding system, annuality with autogamy, and perenniality with allogamy. Such a linkage is also exemplified by Tsitsin’s study on wheat x wheatgrass progeny (Tsitsin 1978). Perenniality together with chasmogamy was always inherited from the wheatgrass parent. However, perenniality also depends in hybrids on a parent genome dosage (Jones et al. 1999) and is expressed as a quantitative trait (Thomas et al. 2000). If linkage between life form and breeding system is strong, then in grass hybrids one can expect new intermediate variation of flowering behaviour, facultative selfing or outcrossing. In annual cereals, common wheat and rye do not support the above linkage.
Variation in dormancy
According to Barrero et al’s considerations (Barrero et al. 2010) dormancy is recognized as a key character of adaptation for a specific ecological niche. Seeds expressing the different levels of dormancy, which are developed on a single plant, probably present the most remarkable pattern of variability. Diaspores can differ in dormancy pattern even in one spikelet, e.g. in wild wheats or oats (Mac Key 1989). In general, dormancy is a complex character created by many genetic-environmental interactions. Light, temperature and water are the most important among environmental factors. The ratio between synthesis of abscisic acid (ABA) and gibberellins (GAs) determines dormancy and germination dynamics. The dormancy genes have been studied in the viviparous maize mutants and the high ABA level barley and rice. The expression of the dormancy genes is also regulated at the epigenetic level (Graeber et al. 2012). Lines with a high level of ABA have also been found in dormant B. distachyon (Barrero et al. 2012). A high level of synthesis of ABA in coleorhizal tissues has been found in barley (Barrero et al. 2009). In the domestication syndrome of plants, dormancy is significantly shortened and cereals are here an example. Wild B. distachyon, a species related to cereals, is a perspective taxon to find new genes of dormancy. A phylogenetic analysis based on the MOTHER OF FT AND TFL1 (MFT) genes proved close relationships between B. distachyon and cereals, wheat and barley (Graeber et al. 2012). The MFT genes, assumed to be a pre-harvest sprouting QTL, are located on chromosome 3 of Triticum aestivum L. (Nakamura et al. 2011). In wheat the dormancy genes (QTL) have also been found on chromosome 4A (Mares et al. 2005). Other dormancy genes have been identified in a wild wheat genome donor, Aegilops tauschii Coss. (Imtiaz et al. 2008). The level of dormancy also depends on the synthesis of phenolic acids, which has been documented in dormant versus pre-harvest sprouting wheat, rye and triticale (Weidner et al. 1999).
A pattern of dormancy variation seen in Fig. 2 (z axis against x + y ones) could probably be interpreted in the form of curvilinear regression of ordination axes; however, its picture (see an insert diagram in Fig. 2) presented for two ordination axes (x and y) is simpler. This variation is presented in the form of a diagonal dotted line of linear regression, extending from zero to maximal values of both axes. The minimal values of ordination axes are characteristic for perennial dormant types, and vice versa, maximal values are represented by non-dormant annuals. As mentioned above, it proves that the main part of dormancy variation shows a distinct trend between two extremes, dormant perennials, and non-dormant annuals.
Variation in grain structure versus dormancy
Bewley and Black (1982) listed several roles attributed to pericarp and testa, which can restrict germination. They include interactions with water uptake and gaseous exchange, the activity of chemical inhibitors, light influence as well as a mechanical effect. For instance, the effect of light on the germination of B. distachyon was evidenced by Barrero et al. (2012). Adkins et al. (2002) highlighted several tissues causing dormancy in the grass diaspore. The decay of coat, as well as glumes and glumellae, removes dormancy. Grzesiuk and Kulka (1988) noted that even a small injury to covering tissues in cereals breaks dormancy. Cutting the testa and pericarp just in the area of the embryo-scutellum, Hou et al. (1997) enabled its rapid imbibition and break of dormancy in Avena fatua. The dormancy can also be expressed as mutifactorial with respect to the grain structure, e.g. in Themeda Forssk. The mechanical and chemical effect of glumellae on caryopsis germination was documented in Hordeum spontaneum (K. Koch) Thell. by Hamidi et al. (2009). Gatford et al. (2002) found some phenolic, i.e. vanillic acid, in bracts of Triticum tauschii (Aegilops tauschii Coss.), which distinctly inhibited germination. These authors suggest that T. tauschii, the D-genome donor to common wheat, can improve cultivated wheats against pre-harvest sprouting. The search for relevant genes should be performed within the available variability of this grass. Phenolics are also common in cereal caryopses (Naczk and Shahidi, 2006). The concentration of ferulic and sinapic acids in dormant cultivars of wheat, rye and triticale is distinctly higher than in those sprouting pre-harvest (Weidner et al. 1999). The phenolic acids (mainly ferulic acid) are linked to the β-glucans in the thick cell walls in the caryopsis of B. distachyon and their contents are similar to other cereals (Guillon et al. 2011). In wheat, β-glucans are synthesized in the cell walls of aleurone as well as subaleurone layers (Shewry et al. 2012). A particularly high concentration of the ferulic acid has been noted in the aleurone cell walls in wheat grain (Parker et al. 2005); however, this phenolic compound is mainly linked not to β-glucans but to arabinoxylan synthesized in the aleurone and transfer area of caryopsis (Robert et al. 2011).
An analysis of the pre-harvest sprouting white versus red wheats has proved that in the white cultivars the tissues of pericarp and integuments are looser and facilitate the rapid imbibition (Huang et al. 1983). However, the study of red seed coat common wheat mutants with white caryopses has shown that the red coat is not obligatory for dormancy expression; however, enhances it (Warner et al. 2000). In addition, Gu et al. (2011) discovered that a pleiotropic gene regulates ABA and flavonoid synthesis in pericarp of red-seeded rice. Such a genetic control makes it difficult to introduce dormancy genes into pre-harvest sprouting cultivars of rice with white pericarp. The ABA and flavonoids were accumulated in the adaxial epidermis of pericarp. In rice, the dormancy feature is even more complex, since the removal of pericarp does not eliminate it completely. Perhaps the most important discovery here is that dormancy alleles are different in tropical and temperate types of weedy rice. Such environment–dormancy relationships have also been well documented in wild barley, Hordeum spontaneum (Yan et al. 2008). Low dormancy was noted in mesic ecotypes, while deep dormancy was seen in xeric populations. The maximum germination ranged between 15 to 103 days. Another comparative genetic analysis of cultivated barley and wild Hordeum spontaneum proved that dormancy is linked to ten genomic regions and that some dormancy genes were lost during the domestication of this crop (Zhang et al. 2005). These results are very important for the consideration of dormancy variation within a set of the wild, weedy and cultivated forms. The wild and weedy forms have been described in B. distachyon (Kosina et al. 2011).
In rice, also the pigment strand, a tissue acting as a gate for the transport of assimilates into endosperm, is highly suberized (Oparka and Gates 1982); and consequently, the tissue acts as a barrier to water uptake and gaseous exchange. The dysfunction of the pigment strand has been evidenced in Aegilops umbellulata Zhuk. (Kosina 2014), while in a Triticeae amphiploid (T. timopheevii (Zhuk.) Zhuk. × Ae. umbellulata) suberization of this area is highly variable (Koźlik 2013).
In addition, several morphs of spikelet rachilla fragility have been detected in B. distachyon (Kosina et al. 2011; Jaroszewicz et al. 2012). This structural variability of a disarticulating scar is within the range of differences between wild and cultivated grasses. Such variability has also been noted in a wild Triticum dicoccoides (Körn. ex Asch. et Graebn.) Schweinf. (Poyarkova et al. 1991) as well as in fatuoid and nonfatuoid Avena sativa L. (Hoekstra et al. 2001). So, one can put a question whether the tissue of the disarticulating scar is variably suberized. If so, then an additional variation in dormancy and germination would be created.
Variation in coleorhizal hairs—a germination structure
The success of germination depends on many components of the diaspore, including some structural ones. One of these are coleorhizal hairs, which are a very special organ of grass caryopsis. They grow on the epidermis of coleorhiza, most often starting on its lateral sides as in Setaria faberi (Haar et al. 2014) and form a capillary sphere around the tip of an embryo. Their water uptake role was accepted a long time ago. In oats, the development of the coleorhizal hairs was distinctly promoted by oxygen (Norstog 1955). So, an aerated and humid capillary soil layer would be the best environment for the development of these hairs. The capillary potential will be larger when many long hairs are densely packed. In cases of high humidity water condenses on these hairs. Rost (1975) assigned the role of water absorption to the coleorhizal hairs in Setaria lutescens (Weigel ex Stuntz) F. T. Hubb. Northam et al. (1996) documented that in Taeniatherum caput-medusae (L.) Nevski from the tribe Triticeae development of coleorhizal hairs strongly depends on the germination temperature. At the end of the first 24 h of germination, at 18 °C, 15–74 % of caryopses had these hairs. Water absorption and seedling anchoring functions have been attributed to them in Taeniatherum Nevski. Their anchoring role has also been documented for many surface-sown grasses (Morita et al. 1997). Bureś (2008) discovered that in two forms of an amphiploid Triticum dicoccum × Aegilops squarrosa (T. dicoccon Schrank. × Ae. tauschii Coss.) the development of coleorhizal hairs expresses distinct variability. An extremely pre-harvest sprouting form with white grains had long and dense hairs, but in another form, expressing no sprouting and having dark grains, the hairs were either poorer or absent. Kosina and Jaroszewicz (2007) presented a significant difference between the development of hairs in B. distachyon and B. sylvaticum. In the former, they are long and abundant. Also, in Setaria faberi the growth of hairs was variable and sometimes they were absent (Haar et al. 2014). Thus, the development of the hairs appears very variable.
In a monocotyledonous seedling, unicellular collar rhizoids create the first active contact between the embryo and the soil and gaseous environment (Tillich 2007). They develop on hypocotyl and coleorhiza and are homologous to the coleorhizal hairs presented here. The collar rhizoids are considered an ancestral character in the family Poaceae. Their absence is treated as a derived state.
The coleorhiza potential for germination is high not only due to water uptake by the hairs, but also via the synthesis of amyloplasts, as has been evidenced in barley (Davidson 1979). This storage capability of coleorhiza is also confirmed by the large amount of protein in the coleorhizal papilla in wheat and its amphiploids (Kosina 1995, 2007).
The variation of the coleorhizal hairs is also expressed as the 0–1 state (absent versus present), e.g. in Secale cereale L. or Aegilops umbellulata (Kosina and Tomaszewska 2014a). A maternal effect on the development of the coleorhizal hairs has been noted in an amphiploid progeny Triticum × Aegilops, reproduced from red or white caryopses (Kosina and Bureś 2014).
Variation in germination
Intra- and interspecific variation in germination
Intraspecific variation is documented by pairs of accessions in each species, for instance Bs1 and Bs2 for B. sylvaticum. Pairs of B. distachyon accessions, TUR2 vs TUR2’ from Turkey and ITA1 vs ITA1’ from Italy, show the influence of environment (years of storage) on germination. Winter and facultatively biennial types of B. distachyon appear to be intermediates between spring ecotypes of this species and the perennial species. The germination average taxonomic distance (the UPGMA method of clustering) is distinctly larger between accessions (populations) of B. distachyon than between populations of perennial species (Kosina and Tomaszewska 2014d)
The size of caryopsis also appears to affect dormancy and germination. The large caryopses in Hordeum spontaneum exhibited shallow dormancy and small ones germinated later (Yan et al. 2008). The same factor can modify germination in B. distachyon, because accessions in our collection vary highly in caryopsis size and assimilate storage potential (Jaroszewicz et al. 2012; Kosina and Kamińska 2013a). De facto, smaller caryopses expressed deeper dormancy (Kosina and Jaroszewicz 2007).
The above data are also important from the point of view of weed science. Some species of Brachypodium can become weeds or invasive plants in the case of today’s climate change. This may relate in particular to B. distachyon (Bakker et al. 2009; Jaroszewicz et al. 2012). For weeds, the germination has to be discontinuous and internally controlled as well as possible in various environments (Baker 1974). Invasive populations of B. distachyon in California are highly differentiated and variation of their dormancy is expressed in the form of completely asynchronous germination (Bakker et al. 2009). Such a pattern of variation is well exemplified in Fig. 9 as well as in Fig. 10 (see the relationships between the percentage of germination and root length).
For Bromus sterilis L. and B. tectorum, which are species similar in their mating system and patterns of variability to the annual B. distachyon, a large interpopulational variation in dormancy has been evidenced; however, their weedy bahaviour was different, irrespective of dormancy similarity (Andersson et al. 2002). Inter-family variation of germination in populations of Bromus tectorum varies, depending on population geographical origin (Allen and Meyer 2002). In general, B. tectorum is considered an obligatory selfer, but occasionally it is cross-pollinated (Thill et al. 1984). Thus, the patterns of germination variation in B. distachyon can be modified, similarly as in B. tectorum, by its chasmogamy (Kosina and Tomaszewska 2012) with the possibility of intra- and interspecific hybridisation, which increases the level of heterozygosity (Kosina and Tomaszewska 2014b). B. tectorum is considered a winter grass (Thill et al. 1984; Beckstead et al. 1996), while in B. distachyon spring and winter forms have been described (Schwartz et al. 2010). Winter ecotypes of B. distachyon have various countries of origin in the Mediterrannean region, from Afghanistan to Italy (Kosina and Tomaszewska 2014c). So, studies into the dormancy in spring, winter and facultatively biennial types of B. distachyon could be particularly valuable for weed science.
Brachypodium distachyon versus B. sylvaticum
The qualitative difference between B. distachyon and B. sylvaticum relates to shallow vs deep dormancy. However, the difference between Bs1 and Bs2 (see Fig. 10) proves that in allogamic B. sylvaticum germination behaviour is also interaccessionally variable. B. distachyon is considered to be a facultatively autogamic unit (Kosina and Tomaszewska 2012), while B. sylvaticum is a self-compatible allogamic species (Khan and Stace 1999). However, data presented by Kłyk (2005) proved that the latter also expressed self-incompatible callosic reactions of pollen tubes. Thus, B. sylvaticum can be recognized as an intermediate species between B. distachyon and highly allogamic and self-incompatible ones, e.g. B. pinnatum (see Fig. 1). The facultative self-incompatibility of B. sylvaticum may facilitate intraspecific hybridization of its distant types. Such hybridization has been noted within invasive populations of this species in North America (Rosenthal et al. 2008). The study of intraspecific and interspecific patterns of dormancy and germination variation in both species (Kosina and Jaroszewicz 2007), and here proves to be particularly important, especially when B. sylvaticum is considered a model species in perennial grasses (Steinwand et al. 2013).
The role of hemicellulosic walls in germination
The accumulation of assimilates in the endosperm is dependent on the status of the transfer tissues (vascular bundle, pigment strand, nucellar projection) in the caryopsis. This transfer complex is highly variable in grasses of young hybrid origin (Kosina 2014). In B. distachyon, the assimilates are mainly stored in the form of starch and protein in endosperm and hemicelluloses in the cell walls of endosperm and nucellus. The ratio between starch, protein and hemicelluloses is intraspecifically variable both in the central endosperm (Kosina and Kamińska 2013b) and in the caryopsis as a whole (Kosina and Kamińska 2013a). The interspecific variation is also significant (Kłyk 2005; Kosina and Jaroszewicz 2007, and here see Fig. 3). In seg barley mutants, a dysfunction of tannin vacuoles results in the phenolic saturation of the transfer complex, its necrosis and the abnormal development of endosperm (Felker et al. 1984, 1985). Such a change in the transfer complex hinders the imbibition of caryopsis across the crease.
The aleurone cell walls in Avena fatua contain non-cellulosic polysaccharides, which have a great water capacity (Raju and Walther 1988). In wheat, these polysaccharides are in the form of β-glucan and arabinoxylan, and the latter is highly saturated with ferulic acid (Robert et al. 2011). The same status of endosperm cell has been documented for B. distachyon; however, in this species, differently than in cereals, the endosperm polysaccharides amount to up to 40 %, at the expense of starch. In B. distachyon the feruloylated arabinoxylan is located in the outer layers of the cell wall (Guillon et al. 2011). In the main temperate cereals, i.e. wheat, rye, oat and rye, the feruloylated arabinoxylan is concentrated in the nucellar epidermis and aleurone layer, while β-glucan is in subaleurone endosperm (Dornez et al. 2011). The different, slowly or quickly germinating, morphs of B. distachyon and B. sylvaticum are variable with respect to the thickness of the suberized testa and nucellar epidermis, and the number of cell rows in the aleurone layer (Kosina and Jaroszewicz 2007). Most likely, this variability is related to the amount of phenolic acid in arabinoxylan in the nucellar epidermis and aleurone cells. Here, it should be added that the aleurone layer develops, especially in hybrid forms, in the form of a mosaic of proteinaceous aleurone and starchy cells (Kosina 2007); then, the amount of ferulic acid will be reduced. This will create a new variation in dormancy and germination.
Both groups of Brachypodium species, annuals and perennials, differ in their levels of allogamy. In B. distachyon, it is more restricted but possible, especially in the form of geitonogamy, due to the chasmogamy of flowers. This variation in breeding system creates the different patterns of dormancy and germination in populations of annuals versus perennials. However, in B. distachyon some winter and facultatively biennial forms are intermediate to the perennials. Both groups also differ with respect to their potential for cell wall hemicelluloses, as used during germination. The level of suberin-phenolic synthesis in the testa, pigment strand and caryopsis attachment is higher in the perennials and, very likely, chemically and physically influences their dormancy. The development of coleorhizal hairs is more variable within a heterozygotic population (an accession) of perennial species. This development also differs between the genus Brachypodium and the cereals of Triticeae. Finally, autogamic B. distachyon could be a good source for the selection of new types in terms of dormancy and germination. Filiz et al. (2009) proposed the expansion of the germ-plasm collection of B. distachyon in order to have its broad variation at our disposal. In such a collection we would also propose to maintain ecotypes exemplifying different dormancy, germination and winter hardiness, in the light of climate change and the present-day invasion of some Brachypodium species as new weeds. This broad variation of dormancy and germination in the germ-plasm collection will enable the study of these characteristics at the populational and mutational level. The species of Brachypodium could be a good model taxa for cereals, as was realized in Arabidopsis Heynh. for dicotyledonous plants by Koornneef et al. (2002).
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