Genome-wide transcriptome analysis reveals molecular pathways involved in leafy head formation of Chinese cabbage (Brassica rapa)

XiaoXue Sun , Ram Kumar Basnet , Zhichun Yan , Johan Bucher , Chengcheng Cai , Jianjun Zhao , Guusje Bonnema

Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) : 130

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Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) :130 DOI: 10.1038/s41438-019-0212-9
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Genome-wide transcriptome analysis reveals molecular pathways involved in leafy head formation of Chinese cabbage (Brassica rapa)
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Abstract

Chinese cabbage plants go through seedling and rosette stages before forming their leafy head. Chinese cabbage plants resemble pak-choi plants at their seedling stage, but in their rosette stage the leaves of Chinese cabbage differentiate, as they increase in size with shorter petioles. In order to understand the molecular pathways that play a role in leafy head formation, transcript abundance of young emerging leaves was profiled during development of two Chinese cabbage genotypes and a single pak-choi genotype. The two Chinese cabbages differed in many aspects, among others earliness, leaf size and shape, leaf numbers, and leafy head shape. Genome-wide transcriptome analysis clearly separated the seedling stages of all three genotypes together with the later stages from pak-choi, from the later developmental stages of both Chinese cabbages (rosette, folding, and heading). Weighted correlation network analysis and hierarchical clustering using Euclidean distances resulted in gene clusters with transcript abundance patterns distinguishing the two Chinese cabbages from pak-choi. Three clusters included genes with transcript abundance affected by both genotype and developmental stage, whereas two clusters showed only genotype effects. This included a genotype by developmental stage cluster highly enriched with the MapMan category photosynthesis, with high expression during rosette and folding in Chinese cabbages and low expression in the heading inner leaves that are not exposed to light. The other clusters contained many genes in the MapMan categories Cell, showing again differences between pak-choi and both Chinese cabbages. We discuss how this relates to the differences in leaf blade growth between Chinese cabbage and pak-choi, especially at the rosette stage. Overall, comparison of the transcriptome between leaves of two very different Chinese cabbages with pak-choi during plant development allowed the identification of specific gene categories associated with leafy head formation.

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XiaoXue Sun, Ram Kumar Basnet, Zhichun Yan, Johan Bucher, Chengcheng Cai, Jianjun Zhao, Guusje Bonnema. Genome-wide transcriptome analysis reveals molecular pathways involved in leafy head formation of Chinese cabbage (Brassica rapa). Horticulture Research, 2019, 6 (1) : 130 DOI:10.1038/s41438-019-0212-9

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References

[1]

He, Y. K. et al. Leafy head formation of the progenies of transgenic plants of Chinese cabbage with exogenous auxin genes. Cell Res. 10, 151 (2000).

[2]

Wang, F. et al. Transcriptome analysis of rosette and folding leaves in Chinese cabbage using high-throughput RNA sequencing. Genomics 99, 299-307 (2012).

[3]

Ke, G. L. Chinese Cabbage Breeding (China Agr. Press, Beijing, China, (2012).

[4]

Zhao, J. et al. Genetic relationships within Brassica rapa as inferred from AFLP fingerprints. Theor. Appl. Genet. 110, 1301-1314 (2005).

[5]

Wang, X. et al. The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43, 1035 (2011).

[6]

Cheng, F. et al. Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea. Nat. Genet. 48, 1218 (2016).

[7]

Kopczak, S. D., Haas, N. A., Hussey, P. J., Silflow, C. D. & Snustad, D. P. The small genome of Arabidopsis contains at least six expressed alpha‐tubulin genes. Plant Cell 4, 539-547 (1992).

[8]

Tanksley, S. D. The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16(suppl 1), S181-S189 (2004).

[9]

Mao, Y. et al. MicroRNA319a-targeted Brassica rapa ssp. pekinensis TCP genes modulate head shape in chinese cabbage by differential cell division arrest in leaf regions. Plant Physiol. 164, 710-720 (2014).

[10]

Sun, X. et al. Genetic analysis of Chinese cabbage reveals correlation between rosette leaf and leafy head variation. Front. Plant Sci. 9, 1455 (2018).

[11]

Wang, F. et al. MicroRNA expression analysis of rosette and folding leaves in Chinese cabbage using high-throughput Solexa sequencing. Gene 532, 222-229 (2013).

[12]

Li, Y. et al. Transcriptome profiling of yellow leafy head development during the heading stage in Chinese cabbage (Brassica rapa subsp. pekinensis). Physiol. Plant. 165, 800-813 (2018).

[13]

Li, Y. et al. Identification of quantitative trait loci for yellow inner leaves in Chinese cabbage (Brassica rapa L. ssp. pekinensis) based on SSR and SRAP markers. Sci. Hortic. 133, 10-17 (2012).

[14]

Ge, Y. et al. Mapping quantitative trait loci for leaf and heading-related traits in Chinese cabbage (Brassica rapa L. ssp. pekinesis). Hortic. Environ. Biotechnol. 52, 494 (2011).

[15]

Yu, X. et al. QTL mapping of leafy heads by genome resequencing in the RIL population of Brassica rapa. PLoS ONE 8, e76059 (2013).

[16]

Inoue, T., Kubo, N., Kondo, T. & Hirai, M. Detection of quantitative trait loci for heading traits in Brassica rapa using different heading types of Chinese cabbage. J. Horticultural Sci. Biotechnol. 90, 311-317 (2015).

[17]

Arias, T. et al. Diversification times among Brassica (Brassicaceae) crops suggest hybrid formation after 20 million years of divergence. Am. J. Bot. 101, 86-91 (2014).

[18]

Kim, M. S. et al. Identification and characterization of the leaf specific networks of inner and rosette leaves in Brassica rapa. Biochem. Biophys. Res. Commun. 490, 821-826 (2017).

[19]

van Bueren, E. T. L. & Struik, P. C. Diverse concepts of breeding for nitrogen use efficiency. A review. Agron. Sustain. Dev. 37, 50 (2017).

[20]

McCormick, A. J., Cramer, M. & Watt, D. A. Sink strength regulates photo-synthesis in sugarcane. New Phytol. 171, 759-770 (2006).

[21]

Ainsworth, E. A. & Bush, D. R. Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol. 155, 64-69 (2011).

[22]

Bihmidine, S. et al. Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Front. Plant Sci. 4, 177 (2013).

[23]

Sakamoto, T. et al. Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat. Biotechnol. 24, 105 (2006).

[24]

Truong, S. K., McCormick, R. F., Rooney, W. L. & Mullet, J. E. Harnessing genetic variation in leaf angle to increase productivity of Sorghum bicolor. Genetics 201, 1229-1238 (2015).

[25]

Opena, R. T., Kuo, C. G., & Voon, J. Y. Breeding and Seed Production of Chinese Cabbage in the Tropics and Subtropics (Asian Vegetable Research and Development Center, 1988).

[26]

Kalve, S., De Vos, D. & Beemster, G. T. Leaf development: a cellular perspective. Front. Plant Sci. 5, 362 (2014).

[27]

Catterou, M. et al. Brassinosteroids, microtubules and cell elongation in Ara-bidopsis thaliana. II. Effects of brassinosteroids on microtubules and cell elongation in the bul1 mutant. Planta 212, 673-683 (2001).

[28]

Cheng, Z., Snustad, D. P. & Carter, J. V. Temporal and spatial expression pat-terns of TUB9, a β-tubulin gene of Arabidopsis thaliana. Plant Mol. Biol. 47, 389-398 (2001).

[29]

Snustad, D. P., Haas, N. A., Kopczak, S. D. & Silflow, C. D. The small genome of Arabidopsis contains at least nine expressed beta‐tubulin genes. Plant Cell 4, 549-556 (1992).

[30]

Chu, B. et al. Two β-tubulin genes, TUB1 and TUB8, of Arabidopsis exhibit largely nonoverlapping patterns of expression. Plant Mol. Biol. 37. 5, 785-790 (1998).

[31]

Uribe, X. et al. Maize α-tubulin genes are expressed according to specific patterns of cell differentiation. Plant Mol. Biol. 37. 6, 1069-1078 (1998).

[32]

Wasteneys, G. O. & Ambrose, J. C. Spatial organization of plant cortical microtubules: close encounters of the 2D kind. Trends Cell Biol. 19, 62-71 (2009).

[33]

Basnet, R. K. et al. Genome-wide analysis of coordinated transcript abundance during seed development in different Brassica rapa morphotypes. BMC Genomics 14, 840 (2013).

[34]

Smyth, G. K. in Bioinformatics and computational biology solutions using R and Bioconductor (Statistics for Biology and Health, 2005).

[35]

Horvath, S. & Dong, J. Geometric interpretation of gene coexpression network analysis. PLoS Comput. Biol. 4, e1000117 (2008).

[36]

Usadel, B. et al. Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of coresponding genes, and comparison with known responses. Plant Physiol. 138, 1195-1204 (2005).

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