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10.1 Diversification of Brassica Species

The rich diversity in phenotypes or morphotypes is the most distinct feature for Brassica plants. There are two levels of diversification for Brassica (Fig. 10.1): (1) Many Brassica species evolved from a common ancestor, and they are close relatives to each other. (2) There are abundant morphotypes for each Brassica species. First, the six main Brassica crops, referred to above, whose relationships were describes by U-triangle (Nagaharu 1935) represent the rich speciation of Brassica. Second, each of these Brassica species evolved into rich varieties with diversified phenotypes, including leafy heads, enlarged roots, other enlarged organs of stems or inflorescences, oilseeds, sarsons, and even ornamental features. In Brassica rapa, heading Chinese cabbage and pak choi are consumed as leafy vegetables. Chinese cabbage is specific for its large leafy head, whereas pak choi has relatively smaller leaves and does not form heading leaves. Turnip has an enlarged root that is edible or occasionally used as fodder. Caixin and purple caitai bolt rapidly and generate long, tender stems used as food. Morphotypes of oilseed B. rapa produce large, full seeds for oil extraction, and sarsons grow seed pods that are eaten in India. Some morphotypes of B. rapa develop beautiful leaf patterns or colors, and are thus used as ornamental plants. Brassica oleracea also has rich morphotypes. Heading B. oleracea is also used as a leaf vegetable, whereas oilseed B. oleracea produces edible oil. Cauliflower and broccoli, special morphotypes of B. oleracea, develop enlarged inflorescences that are eaten as vegetables. Other Brassica crops, such as Brassica juncea, have even greater numbers of rich morphotypes than B. rapa and B. oleracea. In addition to these cultivated crops, there are many wild relatives of the species in U-triangle that have greatly diversified phenotypes, further extending the diversity of Brassica. Additionally, many morphotypes or phenotypes shared among Brassica developed independently and in parallel, such as the heading leaves in B. rapa and B. oleracea, and enlarged roots in B. rapa and B. juncea.

Fig. 1
figure 1

Two levels of diversification for Brassica species following the WGT event. Level 1 is the speciation that occurred during the process of rediploidization and tetraploidization after WGT. Level 2 is the morphotype boom after the speciation, which is likely to have been driven by the biased fractionation of subgenomes, as well as the functional differentiation of multicopy genes generated from WGT

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The whole-genome triplication (WGT) that occurred in the common ancestor of Brassica crops played an important role in the diversification of Brassica plants. It was observed that new plant species always evolve after polyploidization. There are many such events in the evolutionary history of the plant kingdom, such as the diversification of early core eudicots (Jiao et al. 2102) (Lysak et al. 2005; Van de Peer et al. 2009). This process of diversification is also related to the events after whole-genome duplication (WGD), including migrations, the fluctuations in environments, and/or human cultivation/selection (Proost et al. 2011), but polyploidization provides plants with the ability to be diversified and respond to changed habitats. Furthermore, from the aspect of genes, the multicopy genes generated from WGD could develop new functions (gene subfunctionalization or neofunctionalization); thus new traits or morphotypes of plants could evolve. Brassica species shared an additional common feature that they all experienced an extra WGT event, which occurred approximately 9–15 million years ago (MYA) (Beilstein et al. 2010; Wang et al. 2011b) or even approximately 28 MYA (Lukens et al. 2004; Lysak et al. 2005; Arias et al. 2014). The WGT event is important for the speciation and the morphotype expansion of genus Brassica. The subsequent genomic rearrangements and gene evolution initiated by WGT contributed to the booming of a variety of Brassica plants.

10.2 Chromosome Evolution after WGT and the Brassica Speciation

Brassica shared a common WGT event, which has been confirmed by different aspects, such as a comparative genomic analysis (Cheng et al. 2013). Genomic synteny between B. rapa and Arabidopsis thaliana clearly revealed the WGT event experienced by B. rapa (Wang et al. 2011b). Most genes inherited from their nearest common ancestor were shared by B. rapa and A. thaliana (80.2 and 73.8 % for B. rapa or A. thaliana, respectively) (Cheng et al. 2012a, b). Although big genomic fragments were fractionated during the rediploidization of B. rapa, the local gene order was conserved and syntenic fragments can be identified between B. rapa and A. thaliana. For each genomic fragment of A. thaliana, three syntenic copies were found in B. rapa. These three genome copies were generated from the WGT event (Wang et al. 2011b; Cheng et al. 2012b). Furthermore, a synteny analysis between B. oleracea and A. thaliana also showed that B. oleracea had good genomic collinearity with A. thaliana, and B. oleracea shared the same WGT event as that of B. rapa (Liu et al. 2014). Meanwhile, comparative studies of B. juncea and other Brassica using information from linkage maps showed that B. nigra also shared the same WGT event (Panjabi et al. 2008). Furthermore, previous works, including genomic structure analyses, paleocentromere evolution, and phylogenic studies, among multiple genomes of Brassicaceae evidenced that the diploid ancestor of B. rapa resembled the block arrangement of translocation Proto-Calepineae Karyotype (tPCK), which has seven chromosomes (Cheng et al. 2013). Finally, based on this information, we established that all Brassica crops referred to in U-triangle evolved from a common diploid tPCK genome that experienced a WGT event.

Chromosomal reduction and rearrangement, accompanied with paleocentromere descended from the hexaploid ancestor (tPCK × 3, n = 21), were important for the speciation of Brassica plants. After WGT, extensive chromosome reshuffling during rediploidization lead to the origin of closely related species in Brassica. In polyploids, it is understandable that having more than two copies of homologous chromosomes at the synapsis stage of meiosis will result in abnormal synaptonemal complexes, thereby decreasing the fertility of gametes. Logically, natural selection drives the rediploidization process with chromosomal rearrangement that all eliminate the extra homologous chromosomes. Further rounds of genomic reshuffling in the rediploid ancestor at different evolutionary time points then created different species of Brassica (Fig. 10.1). In the genome of B. rapa, chromosomes and paleocentromeres were reduced from 21 to 10 through multichromosome translocation, fusion, and inter/intrachromosomal recombination. These genomic reshuffling events should also have occurred in the origin of other Brassica species.

10.3 Gene Evolution after WGT and the Evolution of Rich Morphotypes in Brassica

Biased gene retention after WGT may promote the diversification of Brassica plants. Phytohormones, especially auxin, play important roles in the morphogenesis of plants (Santner and Estelle 2009). The genes that are involved in phytohormone signaling are thus important for the formation of diversified morphotypes (Gazzarrini and McCourt 2003; Santner and Estelle 2009). By comparing gene categories between B. rapa and other genomes, such as A. thaliana, Carica papaya or Vitis vinifera, it was found that auxin-related genes were expanded in B. rapa (Wang et al. 2011b). Furthermore, analysis on gene categories that retained only one or multiple copies found that genes involved in the response to almost all kinds of phytohormone signaling were significantly over-retained in the genomes of B. rapa (Wang et al. 2011b), as well as in B. oleracea (Liu et al. 2014). These redundant phytohormone related genes should contribute to the morphotype diversification of Brassica plants.

Subgenome dominance was observed among the three subgenomes of B. rapa (Cheng et al. 2012b; Tang et al. 2012). The subgenome dominance effect drove the differentiation of paralogous genes. The following differences related to subgenome dominance were found. (1) One subgenome retained more genes than the other two. It is clearly observed by counting the number of genes within the three reconstructed tPCK subgenomes, since one subgenome has approximately 1.5-times more genes than the other two subgenomes (Wang et al. 2011b; Cheng et al. 2012b). (2) There are more genes located in the over retained subgenome expressed at higher levels than in their paralogs. Using mRNA-Seq data generated for different organs of B. rapa, a comparison of paralogous gene pairs showed that a greater number of genes located in the over retained subgenome are expressed at higher levels than their paralogs in the other two subgenomes (Cheng et al. 2012b). (3) Genes in the dominant subgenome accumulated fewer functional mutations than those of the other subgenomes (Cheng et al. 2012b). The resequencing of different B. rapa morphotypes showed that genes located in the dominant subgenome accumulated fewer functional mutations than those located in the other two subgenomes, which was also considered as the ongoing biased fractionation in B. rapa (Cheng et al. 2012b).

WGT provided redundant genes as materials, or a buffer pool, for multicopy genes to evolve new functions, and the subgenome dominance effect facilitated the process by differentiating the multicopy genes that were located in different subgenomes of B. rapa. The newly evolved functions may promote the evolution of different morphotypes of Brassica species. In A. thaliana, many duplicated genes were subfunctionalized or neofunctionalized after several rounds of whole genome polyploidization, known as the α, β, and γ duplications. For example, genes from extra duplications have become subfunctionalized compared with those in C. papaya, such as the enzymes CYP79A and CYP79B who catalyze the first step of glucosinolate synthesis (Bekaert et al. 2012). Meanwhile, some genes in A. thaliana have become neofunctionalized to develop extra biosynthetic pathways for indole and methionine-derived aliphatic glucosinolates, which do not exist in C. papaya. Glucosinolate genes in B. rapa showed strong over retention after WGT (Wang et al. 2011a). These redundant genes could be subfunctionalization or neofunctionalization to develop new functions of glucosinolate metabolism in B. rapa, as in A. thaliana. It is expected that there are many more overretained genes in B. rapa. The subgenome dominance effect may promote the evolutionary process of these over retained genes by conserving one copy of them and differentiating the other copies to develop new functions. Finally, these differentiated genes will contribute to the evolution of rich B. rapa varieties and similar processes can also occur in other Brassica species.

10.4 Conclusions

A WGT event promoted the diversification of Brassica from two levels represented by speciation and the expansion of rich morphotypes. First, WGT drove the rediploidization process to stabilize the hexaploid genome. Genomic reshuffling and chromosome reduction gave rise to the speciation of diploid Brassica plants as B. rapa, B. nigra, and B. oleracea. The genomic differentiation of the three basic genomes in the U-triangle then generated the stable allotetraploid species such as B. carinata, B. napus, and B. juncea. Second, subgenome differentiation, biased gene retention, and gene subfunctionalization and/or neofunctionalization, after WGT promoted the parallel evolution of many special morphotypes for each Brassica species. Therefore, WGT initialized the genome- and gene-level evolution that further drove the Brassica speciation and generated a bulk of morphotypes for Brassica.

In the near future, further research should be conducted to investigate the evolution of each morphotype of Brassica. Previous studies of whole-genome sequences determined the genome- and gene-level evolution of only one accession of B. rapa. After that, additional B. rapa accessions or other Brassica species should be under extensive study to address the following questions: (1) What are the origins of different morphotypes in Brassicas? (2) What are the mechanisms of parallel evolution of certain morphotypes that developed independently in different Brassica species? (3) Which genes were involved in the development of each morphotype and in the regulation of important agronomic traits in Brassica crops? Answering these questions will increase our knowledge on the diversification of Brassica morphotypes and transfer the benefits of genomic studies to the application of genetic improvement for Brassica crops.