AOBPreview originally published online on March 22, 2004
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Annals of Botany 93: 555-566, 2004
© 2004 Annals of Botany Company
Seed Coat Microsculpturing Changes during Seed Development in Diploid and Amphidiploid Brassica Species
1 Key Laboratory of MOE for Plant Developmental Biology, College of Life Sciences, Wuhan University, Wuhan, 430072, China, 2 College of Medicine and Life Sciences, Jianghan University, Wuhan, 430056, China and 3 Oil Crops Research Institute and The Chinese Agricultural Academy of Sciences, Wuhan, 430062, China
* For correspondence. E-mail jbwang{at}whu.edu.cn
Received: 12 September 2003; Returned for revision: 5 December 2003; Accepted: 19 January 2004 Published electronically: 22 March 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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• Background and Aims Seed coat morphology is known to be an excellent character for taxonomic and evolutionary studies, thus understanding its structure and development has been an important goal for biologists. This research aimed to identify the developmental differences of seed coats between amphidiploids and their putative parents in Brassica.
• Methods Scanning electron microscope (SEM) studies were carried out on six species (12 accessions), three amphidiploids and their three diploid parents.
• Key Results Twelve types of basic ornamentation patterns were recognized during the whole developmental process of the seed coat. Six types of seed coat patterns appeared in three accessions of Brassica rapa, five types in B. oleracea, B. nigra and B. carinata, seven types in B. napus, and eight types in B. juncea. There was less difference among seed coat patterns of the three accessions of B. rapa. The reticulate and blister types were two of the most common patterns during the development of seeds in the six species, the blister-pimple and the pimple-foveate patterns were characteristic of B. rapa, and the ruminate of B. oleracea and B. nigra. The development of seed coat pattern in amphidiploids varied complicatedly. Some accessions showed intermediate patterns between the two putative parents, while others resembled only one of the two parents.
• Conclusions The variation in the patterns of seed coat development could be used to provide a new and more effective way to analyse the close relationship among amphidiploids and their ancestral parents.
Key words: Brassica, amphidiploids, diploids, SEM, seed coat microsculpturing, seed coat development, evolutionary implication.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Polyploidy is widely acknowledged as a major mechanism of adaptation and speciation in higher plants. Recent estimates suggest that 70 % of angiosperms have experienced one or more episodes of polyploidization (Masterson, 1994; Jiang et al., 1998). Various aspects of polyploidy have attracted attention, such as classification of the various types of polyploids, mode and frequency of formation, genetic and genomic attributes of polyploidy, including the immediate and long-term consequences of genome doubling (Wendel, 2000; Liu and Wendel, 2002). However, there is little literature that takes a phylogenetic approach to study the comparative developmental morphology of a trait that exhibits great diversity on both evolutionary and human time-scales (Applequist et al., 2001).
The seed coat (testa) is the interface between the embryo and the exterior environment, and it is a multifunctional organ that plays important roles in embryo nutrition during seed development, and in protection against pests and pathogens from the external environment afterwards (Mohamed-Yasseen et al., 1994; Weber et al., 1996). Most seed coats are derived from the outer and inner integuments of the ovule, composed of a palisade layer, several layers of crushed parenchyma cells and a single layer of aleurone cells (Van Caseele et al., 1982), and they are highly specialized and differentiated to assume several roles at maturity. The seed coat is an essential component in the life-cycle of higher plants.
Based on morphological and anatomical studies (Buth and Ara, 1981; Tobe et al., 1987; Harris, 1991; Sulaiman, 1995; Beeckman et al., 2000), seed coat morphology is known to be an excellent character for taxonomic and evolutionary studies (Vaughan and Whitehouse, 1971; Algan and Baker, 2000; Zou et al., 2001). Thus understanding its structure and development has been an important goal for biologists. At present, seed coat patterns have been used for various purposes: to solve classification problems, to establish evolutionary relationships, to elucidate the adaptive significance of the seed coat, and to serve as genetic markers for the identification of genotypes in segregating hybrid progenies (Lersten, 1979; Gopinathan and Babu, 1985; Rejdali, 1990).
Brassica species have great economic significance for agriculturists because of their value as oilseeds or vegetables, now being the world’s third most important source of vegetable oil (Downey, 1990; Kumar, 1995). Brassica nigra, B. oleracea and B. rapa are the three basic groups that gave rise to three amphidiploid species, B. carinata, B. juncea and B. napus, through the interspecific hybridizations B. nigra x B. oleracea, B. nigra x B. rapa and B. oleracea x B. rapa, respectively (N, 1935; Warwick and Black, 1993). The ovules in Brassica species are bitegmic with each integument two cell layers wide. The epidermis and subepidermis of the seed coat arise from outer and inner cell layers, respectively, of the outer integument. The palisade and parenchymatous layers develop from the two layers of the inner integument of the ovule (Setia and Richa, 1989). Although there is a large body of literature describing the anatomy of mature seed coats of these species (Mulligan and Bailey, 1976; Ren and Bewley, 1998; Koul et al., 2000; Wan et al., 2002), up to now, little has been known about the seed coat patterns during whole seed development in Brassica. Therefore, the present study aimed: (1) to describe the changes in the seed coat at different developmental stages in diploid and amphidiploid Brassica species; and (2) to identify the developmental differences in seed coats between amphidiploids and their putative parents, and to place these differences in an evolutionary context.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plant strains and growth
A list of species along with accessions investigated is given in Table 1. Replete seeds of these accessions were selected and planted in the field at the Oil Crops Research Institute, Chinese Agricultural Academy of Sciences. The accessions of B. oleracea and B. napus were planted in the last 10-d period of September 2002, and others in the last 10-d period of October 2002. They all began to flower at the beginning of April 2003. During flowering stages a nylon netting was used to cover the plants of each accession in order to seclude them from each other and to prevent pollen transfer from one species to another.
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Seed collection and fixation
Flowers were tagged on the days of full anthesis, and each accession had a hundred flowers tagged at the same time. Seed production was ensured by hand pollination. Immature and mature seeds for analysis were collected 5, 10, 15, 20, 25, 30, 35 and 40 d after pollination (DAP), and at the final, full-dry maturity stage. Seeds were fixed in 3 % glutaraldehyde buffered with 0·1 mol L–1 phosphate (pH 7·2) for 3 h at room temperature.
SEM specimens and observation
The seeds were dehydrated through a graduated ethanol series and exchanged in isopentyl acetate. Then they were prepared by critical-point drying, followed by mounting on stubs with double-sided adhesive, sputter coated, and observed on a HITACHI S-450 scanning electron microscope (SEM). For uniformity, the mid-seed and the surface adjacent to the hilum were scanned, and a minimum of six seeds from each accession were examined.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Terminology for the developing seed coat
In this study, the terminology of Murley (1951) was followed, and some extra terms were also added to describe the seed coat microsculpturing (see Table 2). Based on low magnification viewing (x60, x100, x140), the seed surface architecture may be divided into reticulate, foveate, rugose and blister types (Fig. 1). However, at higher magnification (x250, x1000) these types could be further separated into a total of twelve different types: reticulate, foveate, rugose, reticulate-foveate, reticulate-blister, foveolate, blister, pimple, blister-pimple, pimple-foveate, rugose-foveate and ruminate (Figs 2–7). The reticulate type could be split into reticulate, reticulate-foveate, and reticulate-blister, and foveate could be separated into foveate and foveolate. The blister and pimple could each be further divided into two types: blister and blister-pimple, and pimple and pimple-foveate, respectively. Moreover, the rugose could be split into three types: rugose, rugose-foveate and ruminate.
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Five accessions of diploid Brassica were used in this study: three accessions of B. rapa, and one accession of both B. nigra and B. oleracea. Seeds of all three accessions of B. rapa matured at 35 DAP. During the development of the seed coat in these three accessions, there were a total of six types (Figs 2 and 7): reticulate, foveate, blister, blister-pimple, pimple-foveate, and reticulate-foveate. At 5 DAP, the three accessions all showed reticulate type microsculpturing. However, differences appeared among these accessions at 10 and 15 DAP; reticulate and blister in B. rapa 0074, foveate in B. rapa 0113 and pimple-foveate in B. rapa 0265. Brassica rapa 0074 and B. rapa 0113 had the same pattern at 20, 25, 30 and 35 DAP and mature dry seed coat stages: blister-pimple, pimple-foveate, blister, reticulate and reticulate-foveate, respectively. Brassica rapa 0265 had the same patterns as B. rapa 0074 and B. rapa 0113 except that the seed at 35 DAP had a pattern of reticulate-foveate. Hence there was less difference among these accessions of B. rapa during the whole development process of the seed coat than in the other species. The reticulate, blister, blister-pimple and pimple-foveate were the main patterns of the seed coats at different developmental stages.
The maturity time for seed of B. oleracea and B. nigra was 40 DAP and 30 DAP, respectively. Four types of seed coat pattern were observed in B. oleracea during the stages of the seed development: ruminate at 5 DAP, blister at 10, 15 and 25 DAP, reticulate at 20, 30, 35 and 40 DAP, and reticulate-foveate in mature dry seeds (Figs 3 and 7). For wild diploid B. nigra, five types of seed coat architecture appeared during the whole process of seed development: rugose at 10 DAP, ruminate at 15 DAP, blister at 20 and 25 DAP, foveolate at 30 DAP, and reticulate in mature dry seeds (Fig. 3).
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Some interesting patterns were observed during this study of the development of the seed coat. For example, the reticulate, blister, blister-pimple and pimple-foveate types played an important role in the development of the seed coat pattern in B. rapa, whereas the reticulate and blister were the main patterns during the development of seed coat in B. oleracea. Similarly, the rugose and foveolate patterns were important in B. nigra.
Developmental seed coat microsculpturing of amphidiploid Brassica species
Seven accessions of amphidiploid Brassica species were used to study the development of the seed coat: three accessions of B. napus and B. juncea, respectively, and one accession of B. carinata. The maturity time for seeds of B. napus was at 40 DAP, the same time as for the B. oleracea parent. The seeds of B. juncea and B. carinata matured at 35 DAP. For the former this was the same time as for one of its ancestral parents, the latter was intermediate between its ancestral parents (Table 1).
The seed coat patterns of amphidiploids differed from their putative parents. A total of seven types appeared during the development of the seed coat of B. napus (Figs 4 and 7): ruminate, reticulate, reticulate-foveate, blister, pimple-foveate, reticulate-blister and blister-pimple. There was a slight difference among the three accessions at the early developmental stages, but no difference after 30 DAP. For the accession B. napus 2685, six types of seed coat pattern were observed: first the ruminate pattern at 5 DAP, then it changed to reticulate and reticulate-blister, blister-pimple, pimple-foveate, and back to the reticulate-foveate (Figs 4 and 7). The development of the seed coat pattern in B. napus 1256 was reticulate at 5 and 40 DAP, blister at 15, 30 and 35 DAP, reticulate-blister at 10 and 25 DAP, blister-pimple at 20 DAP, and reticulate-foveate in the mature dry seed (Figs 4 and 7). Brassica napus 1219 was nearly consistent with that of B. rapa, one of its ancestral parents, with changes from the reticulate pattern to blister, blister-pimple or pimple-foveate, and then back to the reticulate and reticulate-foveate pattern (Figs 4 and 7). Thus the accession B. napus 2685 appeared to be an integration of its two ancestral parents, B. oleracea and B. rapa, during the overall development of the seed coat. For example, the ruminate type that appeared in B. oleracea at 5 DAP also formed in B. napus 2685 at the same developmental stage, and the pimple-foveate pattern which existed in three accessions of B. rapa also appeared in this amphidiploid accession at 25 DAP. Similarly, B. napus 1219 resembled B. rapa because it had the same pattern of blister-pimple at 20 DAP, and it also resembled B. oleracea in sharing the same reticulate pattern at 35 and 40 DAP and at the mature stage. However, it also had its own particular pattern of reticulate-blister during the development of the seed.
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There were a total of nine types of seed coat during the seed development of B. juncea: reticulate, foveate, reticulate-foveate, ruminate, pimple, pimple-foveate, blister, blister- pimple, and reticulate-blister (Figs 5 and 7). For the accession B. juncea 2194, the developmental seed patterns were similar to B. nigra. For instance, the ruminate appeared at the early stages of seed coat development, just as in B. nigra, and it also resembled B. nigra at the middle and later stages of seed coat development. However, some particular patterns such as blister-pimple, pimple-foveate that appeared in B. rapa at the middle stage of seed development were not observed in the accession. On the contrary, the development of the seed coat pattern of both B. juncea 2316 and B. juncea 0857 were similar to that of B. rapa (such as B. rapa 0074 and 0113), and there were almost no obvious characteristics of B. nigra.
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Brassica carinata was formed through interspecific hybridization between B. nigra and B. oleracea. Five types of seed coat were observed during the whole process of seed development: reticulate-blister, rugose-foveate, blister, reticulate, and rugose (Figs 6 and 7). The rugose and rugose-foveate were the particular patterns for this species. Although the seed coat pattern of mature dry seed was different from its putative parents, seed patterns at a few developmental stages were similar to that of B. oleracea. For example, B. carinata and B. oleracea had almost similar seed patterns from 25–35 DAP. Hence, the seed coat of B. carinata was more similar to that of B. oleracea than that of B. nigra over the whole development process.
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In general, complicated changes in seed coat patterns appeared during seed development in diploid and amphidiploid Brassica species. There were a total of twelve different types in these species, and some common seed coat patterns were observed in different species during a few developmental stages. For example, the reticulate and the blister type often appeared at the early and the later stages. Despite the fact that mature seeds of some species had similar seed coat patterns, different seed coat types appeared in the developmental process (Fig. 7).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Comparison of seed coat patterns among diploids
SEM studies on the seed coat patterns have demonstrated the existence of diversity in various taxa, such as in soybean (Linskens et al., 1977), Goodenia and related genera (Carolin, 1980), Lamiaceae (Rejdali, 1990) and Meconopsis (Sulaiman, 1995). Mature seed coat patterns at high magnification have been found to be species-specific in diploid Brassica species. For example, the type of mature seed coat in all of the four accessions of B. oleracea was observed to be the reticulate pattern (Koul et al., 2000). Our observations of the dry seed of the elementary diploid species were consistent with previous studies (Buth and Ara, 1981; Koul et al., 2000).
Five accessions of diploid Brassica species were studied for the development of the seed coat pattern. The variations in the seed coat patterns observed at higher magnification were generally species-specific, not accession-specific. For example, three accessions of B. rapa resembled each other closely during the whole development of the seed coat. Reticulate or foveate were the main patterns in the early stages (from 5–10 DAP), then the blister, blister-pimple and pimple-foveate were the main patterns in the middle stages (from 15–25 DAP), and the blister, reticulate or reticulate-foveate patterns were the most important in the late stages (from 30 DAP to mature dry seed; Figs 2 and 7). This seems to be the common developmental process of the seed coat pattern in B. rapa. Furthermore, the pimple-foveate and blister-pimple types could be regarded as patterns that are characteristic of seed coat development in B. rapa.
Many patterns observed in B. rapa did not appear in B. oleracea or B. nigra. For example, in the latter two species only the blister and reticulate types formed in the middle stages of seed development, instead of the blister-pimple and pimple-foveate patterns, but they had similar seed patterns in the later stages. On the other hand, some patterns such as the ruminate and the rugose didn’t appear in B. rapa, but they appeared in B. oleracea or B. nigra. The striking change in the seed coat patterns of B. nigra should be noted.
The relationships among B. rapa, B. oleracea and B. nigra have always had a strong appeal to researchers. Based on chloroplast DNA (Warwick and Black, 1991), mitochondrial DNA (Palmer and Herbon, 1988; Pradhan et al., 1992) and nuclear DNA variation (Song et al., 1988a, b, 1990, Yang et al., 1998, 2002), the closeness of B. rapa to B. oleracea and their distinctness from B. nigra has been observed, and diploid Brassica in U’s triangle (N, 1935) can be divided into two evolutionary pathways: the ‘nigra’ lineage and the ‘rapa/oleracea’ lineage (Warwick et al, 1992; Warwick and Black, 1993). The present study failed to supply adequate proof of the closeness of B. rapa to B. oleracea, because B. oleracea had no pimple-foveate and blister-pimple patterns, which were regarded as the characteristic patterns in three accessions of B. rapa during the middle stages of seed development. However, some useful patterns were found that fitted the association over the course of the overall development of the seed. For instance, the seed coat pattern of B. oleracea at 15 DAP is blister, just as that in B. rapa, and the patterns also resembled that of B. rapa in the late stages of seed development. On the other hand, the study did indeed support the distinctiveness of B. rapa from B. nigra.
Evolutionary implications of the seed coat pattern in amphidiploids
Based on the studies on the mature seed coat pattern, Koul et al. (2000) found that four accessions of B. napus had an intermediate pattern, but all eight accessions of B. juncea and one accession of B. napus had a surface pattern resembling one of the two parental diploids, B. rapa. Our observations were in accordance with their observations. The seed coat patterns in amphidiploids could show either an intermediate seed coat pattern between the two putative parents or only one of the two ancestral parents. For the accessions B. napus 1256 and 1219 seed coat patterns were almost consistent with one of their ancestral parents, B. rapa. Similarly, the seed coat patterns of accessions B. juncea 2316 and 0857 also resembled B. rapa over the whole development process, suggesting that these accessions only displayed the characteristics of B. rapa, one of the ancestral parents.
Moreover, some interesting observations could be deduced if the whole development process of the seed is considered. For instance, the seed coat pattern of the accession B. napus 2685 was the same as that of B. oleracea at 5 DAP, although its mature dry seed coat pattern was similar to that of B. rapa (such as 0113 and 0265) and distinct from that of B. oleracea. Similarly, the seed coat pattern of B. juncea 2194 resembled that of B. nigra in the early developmental stages, but its mature dry seed coat patterns were similar to that of B. rapa (such as 0113 and 0265). Therefore, the seed coat pattern in B. napus 2685 and B. juncea 2194 could be a synchronization of the two putative parents if the whole development processis considered.
For B. carinata, Koul et al. (2000) observed two types of mature seed coat, a reticulate and a rugose, and one of the two accessions had a surface pattern resembling only one of the two parental diploids. In the present study, only one accession of B. carinata was used to study the development of the seed coat. Although the mature seed coat pattern was rugose, it displayed a series of changes during the whole development of seed. The seed coat pattern of the mature dry seed was different from both of its ancestral parents, but a few seed coat patterns were similar to those of B. oleracea at a few developmental stages. For example, the seed patterns of B. carinata were almost the same as those in B. oleracea from 25–35 DAP.
Seed coat patterns are primarily determined by inequalities in the heights or projections of outer walls of palisade cells (Vaughan, 1970), or by some pigment deposits in some palisade cells and the formation of polygonal areas around the non-pigmented cells (Buth and Ara, 1981). However, seed coat development appears to undergo an expansive phase followed by many kinds of complicated changes in the outer and inner integuments (Windsor et al., 2000; Wan et al., 2002). The results of these changes, such as production of epidermal mucilage (Bouman, 1975; Van Caseele et al., 1982), and the formation and degradation of starch granules (Windsor et al., 2000; Wan et al., 2002), lead to the distinctive seed coat patterns.
Furthermore, hybrids are established through multiple origins (Song et al., 1988a; Soltis and Soltis, 1999), and seed development is affected by a variety of factors including genetic, physiological and environmental elements (Ren and Bewley, 1998). Developing seeds from reciprocal interploidy crosses often show different phenotypes depending on which parent contributed more chromosomes (Scott et al., 1998), suggesting that maternal and paternal genomes were not functionally equivalent, i.e. different morphotypes of diploids might be involved in the origin of amphidiploids, leading to the resultant variation in seed coat pattern at the intraspecific level (Koul et al., 2000). Thus changes in seed coat patterns in amphidiploids, which derive from the hybridization and chromosome doubling of two putative parents, would become more complicated.
Many genes and mutations affect integument initiation and early development and, as a result, ultimately the pattern of seed coat development. It is therefore important to understand the molecular basics of seed coat development. Recently, some specific genes have been discovered in this field, such as BANYULS (Devic et al., 1999), SCS1 (Batchelorm et al., 2000) and BnCysP1 (Wan et al., 2002), which are expressed in the development of the seed coat. The developmental seed coat patterns of amphidiploids may be better understood once the temporal and spatial expression of these genes are known in more detail.
The seed coat pattern in mature dry seed may be used as a parameter for species identification. However, the present study emphasizes the potential use of the dynamic development of seed coat pattern as an additional parameter that could successfully imply the relationship between diploids and amphidiploids, and could provide a new way to analyse the relationships among different species.
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ACKNOWLEDGEMENTS |
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This work was supported by a grant from National Natural Science Foundation of China [Grant No. 301(0063)].
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LITERATURE CITED |
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-
Algan G, Baker Buyukkartal HN. 2000. Ultrastructure of seed coat development in the natural tetraploid Trifolium pratense L. Journal of Agronomy and Crop Science 184: 205–213.[CrossRef]
Applequist WL, Richard C, Wendel JF. 2001. Comparative development of fiber in wild and cultivated cotton. Evolution and Development 3: 1–13.
Batchelorm AK, Boutilier K, Miller SS, Labbe H, Bowman L, Hu M, Johnson DA, Gijzen M, Miki BLA. 2000. The seed coat-specific expression of a subtilisin-like gene, SCS1, from soybean. Planta 211: 482–492.
Beeckman T, De Rycke R, Viane R, Inze D. 2000. Histological study of seed coat development in Arabidopsis thaliana. Journal of Plant Research 113: 139–148.[CrossRef]
Bouman F. 1975. Integument initiation and testa development in some Cruciferae. The Botanical Journal of the Linnean Society 70: 213–299.
Buth GM, Roshan Ara. 1981. Seed coat anatomy of some cultivated Brassica. Phytomorphology 31: 69–78.
Carolin RC. 1980. Pattern of seed surface of Goodenia and related genera. Australian Journal of Botany 28: 123–137.[CrossRef]
Devic M, Guilleminot J, Debeaujon I, Bechtold N, Bensaude E, Koornneef M, Pelletier G, Delseny M. 1999. The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. The Plant Journal 19: 387–398.[CrossRef][Web of Science][Medline]
Downey RK. 1990. Brassica oilseed breeding: achievements and opportunities. Plant Breeding Abstracts 60: 1165–1170.
Gopinathan MC, Babu CR. 1985. Structural diversity and its adaptive significance in seeds of Vigna minima (Roxb). Ohwi & Ohashi and its allies (Leguminosae-Papilionoideae). Annals of Botany 56: 723–732.
Harris WM. 1991. Seed coat development in radish (Raphanus sativus L.). Phytomorphology 41: 341–349.
Jiang CX, Wright R, El-Zik K, Paterson AH. 1998. Polyploid formation created unique avenues for response to selection in Gossypium (cotton). Proceedings of the National Academy of Science of the USA 95: 4419–4424.
Koul KK, Ranjna Nagpal, Raina SN. 2000. Seed coat microsculpturing in Brassica and allied genera (subtribes Brassicinae, Raphaninae, Moricandiinae). Annals of Botany 86: 385–397.
Kumar D. 1995. Salt tolerance in oilseed Brassicas: present status and future prospects, Plant Breeding Abstracts 65: 1438–1447.
Lersten NR. 1979. A distinctive seed coat pattern in the Viceaceae (Papilionoideae, Leguminoseae). Proceedings of the Iowa Academy of Science 86: 102–104.
Linskens HF, Pfahler PL, Knuiman EL. 1977. Identification of soybean cultivars by the surface relief of the seed-coat. Theoretical and Applied Genentics 50: 147–150.
Liu B, Wendel JF. 2002. Non-Mendelian phenomena in allopolyploid genome evolution. Current Genomics 6: 1–17.
Masterson J. 1994. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264: 421–424.
Mohamed-Yasseen Y, Barringer SA, Splittstoesser WE, Costanza S. 1994. The role of seed coats in seed viability. Botany Review 60: 426–439.
Mulligan GA, Bailey LG. 1976. Seed coat of some Brassica and Sinapis weedy and cultivated in Canada. Economic Botany 30: 143–148.
Murley MR. 1951. Seeds of the Cruciferae of North Eastern America. American Middle Naturalichen 46: 1–81.[CrossRef]
N U. 1935. Genome analysis in Brassica with species reference to the experimental formation of B. napus and peculiar mode of fertilization. Japanese Journal of Botany 7: 389–452.
Palmer JD, Herbon LA. 1988. Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. Journal of Molecular Evolution 28: 87–97.[CrossRef][Web of Science][Medline]
Pradhan SK, Prakash S, Mukhopadhyay A, Pental D.1992. Phylogeny of Brassica and allied genera based on variation in chloroplast and mitochondrial DNA patterns: molecular and taxonomic classifications are incongruous. Theoretical and Applied Genetics 85: 331–340.
Rejdali M. 1990. Seed morphology and taxonomy of the north African species of Sideritis L. (Lamiaceae). Botanical Journal of the Linnean Society 103: 317–324.
Ren CW, Bewley JD. 1998. Seed development, testa structure and precocious germination of Chinese cabbage (Brassica rapa subsp. pekinensis). Seed Science Research 8: 385–397.
Scott RJ, Spielman M, Bailey J, Dickinson HG, 1998. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125: 3329–3341.[Abstract]
Setia RC, Richa. 1989. Anatomical studies on siliqua wall and seed coat development in Brassica juncea (L.) Czern & Coss. Phytomorphology 39: 371–377.
Soltis DE, Soltis P S. 1999. Polyploidy: recurrent formation and genome evolution. Trends in Ecology and Evolution 9: 348–352.
Song KM, Osborn TC, Williams PH. 1988a. Brassica taxonomy based on nuclear restriction fragment length polymorphisms (RFLPs). 1. Genome evolution of diploid and amphidiploid species. Theoretical and Applied Genetics 75: 784–794.
Song KM, Osborn TC, Williams PH. 1988b. Brassica taxonomy based on nuclear restriction fragment length polymorphisms (RFLPs). 2. Preliminary analysis of subspecies within B. rapa (syn. campestris) and B. oleracea. Theoretical and Applied Genetics 76: 593–600.
Song KM, Osborn TC, Williams PH. 1990. Brassica taxonomy based on nuclear restriction fragment length polymorphisms (RFLPs). 3. Genome relationships in Brassica and related genera and the origin of B. oleracea and B. rapa (syn. campestris). Theoretical and Applied Genetics 79: 497–506.
Sulaiman IM. 1995. Scanning electron microscopic studies on seed coat patterns of five endangered Himalayan species of Meconopsis (Papaveraceae). Annals of Botany 76: 323–326.
Tobe H, Wagner WL, Chin Hui-Chen. 1987. A systematic and evolutionary study of Oenothera (Onagraceae): seed coat anatomy. Botanical Gazette 148: 235–257.[CrossRef]
Van Caseele L , Mills JT, Sumner M, Gillespie R. 1982. Cytological study of palisade development in the seed coat of Candle canola. Canadian Journal of Botany 60: 2469–2475.
Vaughan JG. 1970. The structure and utilization of oil seeds. London: Academic Press.
Vaughan JG, Whitehouse JM. 1971. Seed structure and the taxonomy of the Cruciferae. Botanical Journal of the Linnean Society 64: 383–409.
Wan L, Xia Q, Qiu X, Gopalan Selvaaraj. 2002. Early stages of seed development in Brassica napus: a seed coat-specific cysteine proteinase associated with programmed cell death of the inner integument. The Plant Journal 30: 1–10.[CrossRef][Web of Science][Medline]
Warwick SI, Black LD. 1991. Molecular systematics of Brassica and allied genera (subtribe Brassicinae, Brassiceae): chloroplast genome and cytodeme congruence. Theoretical and Applied Genetics 82: 81–92.
Warwick SI, Black LD. 1993. Molecular relationships in subtribe Brassicinae (Cruciferae, tribe Brassiceae). Canadian Journal of Botany 71: 906–918.
Warwick SI, Black LD, Aguinagalde I. 1992. Molecular systematics of Brassica and allied genera (subtribe Brassicinae, Brassiceae): chloroplast DNA variation in the genus Diplotaxis. Theoretical and Applied Genetics 83: 839–850.
Weber H, Borisjuk L, Wobus U. 1996. Controlling seed development and seed size in Vicia faba: a role for seed coat associated invertases and carbohydrate state. The Plant Journal 10: 823–834.[CrossRef][Web of Science]
Wendel JF. 2000. Genome evolution in polyploids. Plant Molecular Biology 42: 225–249.[CrossRef][Web of Science][Medline]
Western TL, Skinner DJ, Haughn GW. 2000. Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiology 122: 345–356.
Windsor JB, Symonds VV, Mendenhall J, Lloyd AM. 2000. Arabidopsis seed coat development: morphological differentiation of the outer integument. The Plant Journal 22: 483–493.[CrossRef][Web of Science][Medline]
Yang YW, Tai PY, Chen Y, Li WH. 2002. A study of the phylogeny of Brassica rapa, B. nigra, Raphanus sativus, and their related genera using noncoding regions of chloroplast DNA. Molecular Phylogenetics and Evolution 23: 268–275.[CrossRef][Web of Science][Medline]
Yang YW, Tseng PF, Tai PY, Chang C J. 1998. Phylogenetic position of Raphanus in relation to Brassica species based on 5S rRNA spacer sequence data. Botanical Bulletin of Academia Sincia 39: 153–160.
Zou X, Foutain DW, Morgan ER. 2001. Anatomical and morphological studies of seed development in Sandersonia aurantiaca Hook. South African Journal of Botany 67: 183–192.
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