Hormones and carbohydrates synergistically regulate the formation of swollen roots in a Chinese cabbage translocation line

Xiaojing Ren , Wei Ma , Shuxin Xuan , Dandan Li , Yanhua Wang , Yuanchao Xu , Daling Feng , Jianjun Zhao , Xueping Chen , Shuangxia Luo , Shuxing Shen , Aixia Gu

Horticulture Research ›› 2023, Vol. 10 ›› Issue (8) : 121

PDF (4343KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (8) :121 DOI: 10.1093/hr/uhad121
Article
research-article
Hormones and carbohydrates synergistically regulate the formation of swollen roots in a Chinese cabbage translocation line
Author information +
History +
PDF (4343KB)

Abstract

The genus Brassica contains a rich diversity of species and morphological types, including leaf, root, and oil crops, all of which show substantial phenotypic variation. Both Chinese cabbage and cabbage are typical leaf-type crops with normal roots. We created translocation lines based on interspecific crosses between Chinese cabbage and cabbage and identified qdh225, which exhibited a swollen-root phenotype. The swollen root of qdh225 contained a large number of granular substances, and the formation of its irregular morphological tissue was caused by a thickening of the phloem. Transcriptomic and metabolomic data suggested that differential expression of genes encoding nine types of enzymes involved in starch and sucrose metabolism caused changes in starch synthesis and degradation in the swollen root. These genes jointly regulated sucrose and starch levels, leading to significant enrichment of starch and soluble proteins in the swollen root and a reduction in the content of soluble sugars such as d-glucose and trehalose 6-phosphate. A significant increase in auxin (IAA) and abscisic acid (ABA) contents and a decrease in gibberellin (GA) content in the swollen root likely promoted the differential expression of genes associated with hormone signal transduction, thereby regulating the development of the swollen root. Taken together, our data suggest that accumulation of IAA and ABA and reduction in GA promote swollen root formation by regulating hormone-mediated signaling, leading to a thickening of phloem, root enlargement, and substantial accumulation of starch and soluble proteins. The latter provide materials, energy, and nutrient sources for the development of swollen roots.

Cite this article

Download citation ▾
Xiaojing Ren, Wei Ma, Shuxin Xuan, Dandan Li, Yanhua Wang, Yuanchao Xu, Daling Feng, Jianjun Zhao, Xueping Chen, Shuangxia Luo, Shuxing Shen, Aixia Gu. Hormones and carbohydrates synergistically regulate the formation of swollen roots in a Chinese cabbage translocation line. Horticulture Research, 2023, 10 (8) : 121 DOI:10.1093/hr/uhad121

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 31930098 and 32172560), the Hebei Provincial Natural Science Fund for Distinguished Young Scholars (Grant No. C2020204063), and the Innovative Research Group Project of Hebei Natural Science Foundation (Grant No. C2020204111). We appreciate the linguistic assistance provided by A&L Scientific Editing (www.alpublish.com) during the preparation of this manuscript.

Author contributions

S.S., A.G., W.M., and S.X. conceived and designed the experiment; X.R., D.L., and Y.X. carried out the experiments; X.R., W.M., S.X., Y.W., D.F., J.Z., X.C., and S.L. analyzed data; X.R. and W.M. prepared the manuscript; X.R., W.M., S.X., A.G., and S.S. wrote the paper; and all of the authors read and approved the final manuscript.

Data availability

The RNA-seq datasets for qdh225 and 85-1 have been deposited at the NCBI Sequence Read Archive under accession number PRJNA913444.

Conflict of interest

The authors have no conflict of interest to declare.

References

[1]

Villordon AQ, Ginzberg I, Firon N . Root architecture and root and tuber crop productivity. Trends Plant Sci. 2014; 19: 419-25.

[2]

Zhang L, Li Z, Garraway J et al. The casein kinase 2 β subunit CK2B1 is required for swollen stem formation via cell cycle control in vegetable Brassica juncea . Plant J. 2020; 104: 706-17.

[3]

Yang LM, Fang ZY, Zhang YY et al. Recent advances of disease and stress resistance breeding of cabbage in China. Acta Hortic Sin. 2020; 47: 1678-88.

[4]

Zhang YY, Fang ZY et al. A new winter cabbage hybrid ‘Zhonggan 1305’. Acta Hortic Sin. 2020; 47: 607-8.

[5]

Zhang J, Zhang JP, Liu WH et al. An intercalary translocation from Agropyron cristatum 6P chromosome into common wheat confers enhanced kernel number per spike . Planta. 2016; 244: 853-64.

[6]

Cai D, Kleine M, Kifle S et al. Positional cloning of a gene for nematode resistance in sugar beet. Science. 1997; 275: 832-4.

[7]

Cao QH et al. Identification and characterization of a cucumber alien translocation line CT-01 possessing resistance to downy mildew. Acta Hortic Sin. 2008; 32: 1098-101.

[8]

Ikeda H, Hiraga M, Shirasawa K et al. Analysis of a tomato introgression line, IL8-3, with increased Brix content. Sci Hortic. 2013; 153: 103-8.

[9]

Wang H, Yu Z, Li G et al. Diversified chromosome rearrangements detected in a wheat- Dasypyrum breviaristatum substitution line induced by gamma-ray irradiation . Plants. 2019; 8: 175.

[10]

Dai KL, Zhao RH, Shi MM et al. Dissection and cytological mapping of chromosome arm 4VS by the development of wheat- Haynaldia villosa structural aberration library . Theor Appl Genet. 2019; 133: 217-26.

[11]

Chen P, You C, Hu Y et al. Radiation-induced translocations with reduced Haynaldia villosa chromatin at the Pm21 locus for powdery mildew resistance in wheat . Mol Breed. 2013; 31: 477-84.

[12]

Knott DR . Transferring alien genes to wheat. In: Heyne EG (ed.), Wheat and Wheat Improvement , Vol. 13. Saskatoon: University of Saskatchewan, 1987, 462-71.

[13]

Islam A, Shepherd KW . Production of wheat-barley recombinant chromosomes through induced homoeologous pairing. Theor Appl Genet. 1992; 83: 489-94.

[14]

Li GR, Liu C, Li CH et al. Introgression of a novel Thinopyrum intermedium St-chromosome-specific HMW-GS gene into wheat . Mol Breed. 2013; 31: 843-53.

[15]

Xie W, Ben-David R, Zeng B et al. Suppressed recombination rate in 6VS/6AL translocation region carrying the Pm21 locus introgressed from Haynaldia villosa into hexaploid wheat. Mol Breed. 2012; 29: 399-412.

[16]

Li A, Jiang JJ, Zhang YT et al. Molecular and cytological characterization of introgression lines in yellow seed derived from somatic hybrids between Brassica napus and Sinapis alba . Mol Breed. 2012; 29: 209-19.

[17]

Luo WL, Guo JX et al. Study on microspore culture-based haploid breeding technology of Chinese kale (Brassica oleracea). Guangdong Agric Sci. 2020; 47: 36-43.

[18]

Sun YY, Li XX . A review on molecular mechanism of the modified roots or stems development in vegetables. Sci Agric Sin. 2015; 48: 1162-76.

[19]

Kloosterman B, Navarro C, Bijsterbosch G et al. StGA2ox1 is induced prior to stolon swelling and controls GA levels during potato tuber development. Plant J. 2007; 52: 362-73.

[20]

Sun Q, Zhou G, Cai Y et al. Transcriptome analysis of stem development in the tumourous stem mustard Brassica juncea var. tumida Tsen et Lee by RNA sequencing . BMC Plant Biol. 2013; 13: 90.

[21]

Pasare SA, Ducreux LJM, Morris WL et al. The role of the potato (Solanum tuberosum) CCD8 gene in stolon and tuber development . New Phytol. 2013; 198: 1108-20.

[22]

Wang W, Gong YQ, Liu LW et al. Changes of sugar content and sucrose metabolizing enzyme activities during fleshy taproot development in radish (Raphanus sativus L.). Acta Hortic Sin. 2009; 34: 1313-6.

[23]

Lutova LA, Dolgikh EA, Dodueva IE et al. Investigation of systemic control of plant cell division and differentiation in the model of tumor growth in radish. Russian J Genet. 2008; 44: 936-43.

[24]

Shi H, Wang LL, Sun LT et al. Cell division and endoreduplication play important roles in stem swelling of tuber mustard (Brassica juncea Coss. var. tumida Tsen et lee). Plant Biol. 2012; 14: 956-63.

[25]

García MNM, Giammaria V, Grandellis C et al. Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta. 2012; 235: 761-78.

[26]

Xu YC . Identification of Chinese Cabbage-Cabbage Translocation Lines with Fragment of Cabbage Chromosome 4 and Analysis of Related Traits. Baoding: Hebei Agricultural University; 2016.

[27]

Roumeliotis E, Visser RGF, Bachem CWB . A crosstalk of auxin and GA during tuber development. Plant Signal Behav. 2012b; 7: 1360-3.

[28]

Wang QM, Zhang LM, Wang ZL . Formation and thickening of tuberous roots in relation to the endogenous hormone concentrations in sweet potato. Sci Agric Sin. 2005; 38: 2414-20.

[29]

Slugina MA, Boris KV, Kakimzhanova AA et al. Intraspecific polymorphism of the sucrose synthase genes in Russian and Kazakhstan potato cultivars. Genetika. 2015; 50: 677-82.

[30]

Marchant A, Bhalerao R, Casimiro I et al. AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell. 2002; 14: 589-97.

[31]

Zhou J, Wen ZW, Mei YY et al. The mechanism underlying the role of SAUR72 in Arabidopsis leaf senescence regulation. Plant Physiol J. 2018; 54: 379-85.

[32]

Ariizumi T, Murase K, Sun TP et al. Proteolysis-independent downregulation of DELLA repression in Arabidopsis by the GIBBERELLIN receptor GIBBERELLIN INSENSITIVE DWARF1 . Plant Cell. 2008; 20: 2447-59.

[33]

Ueguchi-Tanaka M, Ashikari M, Nakajima M et al. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature. 2005; 437: 693-8.

[34]

Ubeda-Tomás S, Swarup R, Coates J et al. Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis . Nat Cell Biol. 2008; 10: 625-8.

[35]

García MNM, Stritzler M, Capiati DA . Heterologous expression of Arabidopsis ABF4 gene in potato enhances tuberization through ABA-GA crosstalk regulation . Planta. 2014; 239: 615-31.

[36]

Antoni R, Gonzalez-Guzman M, Rodriguez L et al. PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiol. 2013; 161: 931-41.

[37]

Fujii H, Verslues PE, Zhu JK . Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis . Plant Cell. 2007; 19: 485-94.

[38]

Li Y, Jones L, McQueen-Mason S . Expansins and cell growth. Curr Opin Plant Biol. 2003; 6: 603-10.

[39]

Francis D. The plant cell cycle-15 years on. New Phytol. 2007; 174: 261-78.

[40]

Wu Y, Zhang S, Zhang H et al. QTL mapping and candidate gene identification of swollen root formation in turnip. Int J Mol Sci. 2021; 22: 653.

[41]

Dong LL . Anatomical and cytological studies on stem swelling in Brassica juncea var. tumida Tsen et Lee. Master’s Thesis. Zhejiang University; 2010.

[42]

Smolarkiewicz M, Dhonukshe P . Formative cell divisions: principal determinants of plant morphogenesis. Plant Cell Physiol. 2013; 54: 333-42.

[43]

Geigenberger P. Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot. 2003; 54: 457-65.

[44]

Fernie AR, Willmitzer L . Molecular and biochemical triggers of potato tuber development. Plant Physiol. 2001; 127: 1459-65.

[45]

Shewry PR . Tuber storage proteins. Ann Bot. 2003; 91: 755-69.

[46]

Tsai WY, Jheng YJ, Chen KH et al. Molecular cloning, structural analysis and mass spectrometric identification of native dioscorins of various yam species. J Sci Food Agric. 2013; 93: 761-70.

[47]

Gray WM . Hormonal regulation of plant growth and development. PLoS Biol. 2004; 2: e311.

[48]

Roumeliotis E, Kloosterman B, Oortwijn M et al. The effects of auxin and strigolactones on tuber initiation and stolon architecture in potato. J Exp Bot. 2012; 63: 4539-47.

[49]

Aung LH . Growth substances and environment on the development of vegetative storage organs. In:In: Purohit SS (ed.), Hormonal Regulation of Plant Growth and Development. Agro Botanical Publishers: Bikaner, 1990, 91-106.

[50]

Mitsui Y, Shimomura M, Komatsu K et al. The radish genome and comprehensive gene expression profile of tuberous root formation and development. Sci Rep. 2015; 5: 10835.

[51]

Wang S, Wang X, He Q et al. Transcriptome analysis of the roots at early and late seedling stages using Illumina paired-end sequencing and development of EST-SSR markers in radish. Plant Cell Rep. 2012; 31: 1437-47.

[52]

Cheng L, Li S, Yin J et al. Genome-wide analysis of differentially expressed genes relevant to rhizome formation in lotus root (Nelumbo nucifera Gaertn). PLoS One. 2013; 8: e67116.

[53]

Lou P, Zhao J, Kim JS et al. Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa . J Exp Bot. 2007; 58: 4005-16.

[54]

Kubo N, Saito M, Tsukazaki H et al. Detection of quantitative trait loci controlling morphological traits in Brassica rapa L. Breed Sci. 2010; 60: 164-71.

[55]

Hashida T, Nakatsuji R, Budahn H et al. Construction of a chromosome-assigned, sequence-tagged linkage map for the radish, Raphanus sativus L. and QTL analysis of morphological traits . Breed Sci. 2013; 63: 218-26.

[56]

Lu G, Cao J, Yu X et al. Mapping QTLs for root morphological traits in Brassica rapa L. based on AFLP and RAPD markers . J Appl Genet. 2008; 49: 23-31.

[57]

Tong NK, Chen S . Genetic studies on some important characters of vegetable mustard. Acta Hortic Sin. 1992; 19: 151-6.

[58]

Ramchiary N, Padmaja KL, Sharma S et al. Mapping of yield influencing QTL in Brassica juncea: implications for breeding of a major oilseed crop of dryland areas . Theor Appl Genet. 2007; 115: 807-17.

[59]

Lu J, Wang L . Problems and solutions in paraffin section making. Preclin Med Educ Edn. 2001; 3: 263.

[60]

Zhang YY, Chen LB . Observation of the structure of tobacco leaf tissue with SEM. J Chin Electron Microsc Soc. 2000; 19: 154-7.

[61]

Tang LQ, Li C, Liu S et al. Determination of pachyman in Radix ophiogonis content by anthrone-sulphuric acid colorimetry . Anhui Med Pharm J. 2003; 7: 39-40.

[62]

Yue SY, Zhou RR, Nan TG et al. Comparison of major chemical components in Puerariae thomsonii radix and Puerariae lobatae radix . China J Chin Mater Med. 2022; 47: 2689-97.

[63]

Jiao J . Determination of soluble protein content in alfalfa by Coomassie brilliant blue G-250 staining. Agric Eng Technol. 2016; 36: 33-4.

[64]

Zhang WB, He JL, Jiang H et al. Determination of cellulose and hemicellulose in lignocellulosic materials. Jiangsu Agric Sci. 2017; 45: 281-4.

[65]

Sun KY, Chen Y . Analytical methods of endogenous phytohormone. Hubei Agric Sci. 2011; 50: 3681-3.

[66]

He ZP . Experimental Guidance by Chemical Control of Crop. Beijing: Beijing Agricultural University Press; 1993.

[67]

Shi J, Ma WJ, Wang C et al. Impact of various microbial-fermented methods on the chemical profile of dark tea using a single raw tea material. J Agric Food Chem. 2021; 69: 4210-22.

PDF (4343KB)

69

Accesses

0

Citation

Detail

Sections
Recommended

/