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Carbohydrate, phytohormone, and associated transcriptome changes during storage root formation in alligatorweed (Alternanthera philoxeroides)

Published online by Cambridge University Press:  11 May 2020

Junliang Yin Open the ORCID record for Junliang Yin [Opens in a new window] ,
Jie Tian ,
Gang Li ,
Yongxing Zhu ,
Xiaokang Zhou ,
Yang He ,
Peiyao Nie ,
Yanmeng Su ,
Qiwen Zhong  and
Zhongyi Chen
Junliang Yin
Affiliation:
Researcher, Academy of Agriculture and Forestry Sciences of Qinghai University (Qinghai Academy of Agriculture and Forestry Sciences), Qinghai Key Laboratory of Vegetable Genetics and Physiology, State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, China Researcher, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Yangtze University, Jingzhou, China
Jie Tian
Affiliation:
Researcher, Academy of Agriculture and Forestry Sciences of Qinghai University (Qinghai Academy of Agriculture and Forestry Sciences), Qinghai Key Laboratory of Vegetable Genetics and Physiology, State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, China
Gang Li
Affiliation:
Researcher, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Yangtze University, Jingzhou, China
Yongxing Zhu
Affiliation:
Researcher, Academy of Agriculture and Forestry Sciences of Qinghai University (Qinghai Academy of Agriculture and Forestry Sciences), Qinghai Key Laboratory of Vegetable Genetics and Physiology, State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, China Researcher, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Yangtze University, Jingzhou, China
Xiaokang Zhou
Affiliation:
Researcher, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Yangtze University, Jingzhou, China
Yang He
Affiliation:
Researcher, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Yangtze University, Jingzhou, China
Peiyao Nie
Affiliation:
Researcher, Biomarker Technologies, Beijing, China
Yanmeng Su
Affiliation:
Researcher, Suzhou Grace Biotechnology Co. Ltd., Suzhou, China
Qiwen Zhong*
Affiliation:
Professor, Academy of Agriculture and Forestry Sciences of Qinghai University (Qinghai Academy of Agriculture and Forestry Sciences), Qinghai Key Laboratory of Vegetable Genetics and Physiology, State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, China
Zhongyi Chen*
Affiliation:
Professor, Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Yangtze University, Jingzhou, China
*
Authors for correspondence: Qiwen Zhong, State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining810016, China. (Email: [email protected]) Zhongyi Chen, College of Horticulture and Gardening, Yangtze University, Jingzhou434000, Hubei, China. (Email: [email protected])
Authors for correspondence: Qiwen Zhong, State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining810016, China. (Email: [email protected]) Zhongyi Chen, College of Horticulture and Gardening, Yangtze University, Jingzhou434000, Hubei, China. (Email: [email protected])
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Abstract

The storage root of alligatorweed [Alternanthera philoxeroides (Mart.) Griseb.] growing in terrestrial habitats is an important metamorphic organ for its propagation, overwintering, and spread. However, the regulatory mechanism adventitious root expansion to form storage roots is still unclear. To reveal the changes accompanying the root-swelling process, we quantified sugar, soluble protein, and phytohormone content in adventitious and storage roots. Results demonstrated that sucrose, fructose, and soluble protein increased in storage roots, whereas abscisic acid (ABA), indoleacetic acid (IAA), brassinosteroid (BR), gibberellin, jasmonic acid, and cytokinin (trans-zeatin [tZ] and isopentenyladenine [iP] and the corresponding ribosides tZR and iPR). tZ-type (tZR and tZ) content decreased, suggesting the involvement of sugars and hormones in the formation of storage roots. To further reveal the molecular basis of A. philoxeroides’s ability to form storage roots and provide candidate genes for molecular function analyses, we assembled a de novo transcriptome of A. philoxeroides based on four sets of RNA-sequencing data. According to functional annotation and expression profiling, 42 unigenes involved in sucrose synthesis and hydrolysis were identified, in addition to 70, 58, and 78 unigenes in ABA, BR, and IAA signal transduction, respectively. The quantitative reverse transcriptase polymerase chain reaction analysis revealed 21 unigenes involved in sugar metabolism and hormone signal transduction were differentially expressed during the formation of storage roots. These results revealed metabolic changes during the formation of storage roots and provide candidate genes involved in sugar and phytohormone metabolism in A. philoxeroides.

Keywords

Alligator weedbioinformaticssignaling transductionsugar metabolismroot swelling
Type
Research Article
Information
Weed Science , Volume 68 , Issue 4 , July 2020 , pp. 382 - 395
Copyright
© Weed Science Society of America, 2020

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Footnotes

Associate Editor: William Vencill, University of Georgia

*

These authors contributed equally to this work.

References

Amini, F, Ehsanpour, AA (2005). Soluble proteins, proline, carbohydrates and Na+/K+ changes in two tomato (Lycopersicon esculentum Mill.) cultivars under in vitro salt stress. Am J Biochem Biotech 1:204–208Google Scholar
Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
Bolger, AM, Lohse, M, Usadel, B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle ScholarPubMed
Castleden, CK, Aoki, N, Gillespie, VJ, MacRae, EA, Quick, WP, Buchner, P, Foyer, CH, Furbank, RT, Lunn, JE (2004) Evolution and function of the sucrose-phosphate synthase gene families in wheat and other grasses. Plant Physiol 135:1753–1764CrossRefGoogle ScholarPubMed
Chandler, JW (2016) Auxin response factors. Plant Cell Environ 39:1014–1028CrossRefGoogle ScholarPubMed
Chen, Z, Xiong, Z, Pan, X, Shen, S, Geng, Y, Xu, C, Chen, J, Zhang, W (2015) Variation of genome size and the ribosomal DNA ITS region of Alternanthera philoxeroides (Amaranthaceae) in Argentina, the USA, and China. J Syst Evol 53:82–87CrossRefGoogle Scholar
Clouse, SD (2012) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23:1219–1230CrossRefGoogle Scholar
Cyr, DR, Derek, BJ (1990) Proteins in the roots of the perennial weeds chicory (Cichorium intybus L.) and dandelion (Taraxacum officinale Weber) are associated with overwintering. Planta 182:370–374CrossRefGoogle ScholarPubMed
Di, F, Jian, H, Wang, T, Chen, X, Ding, Y, Du, H, Lu, K, Li, J, Liu, L (2018) Genome-wide analysis of the PYL gene family and identification of PYL genes that respond to abiotic stress in Brassica napus. Genes 9:156CrossRefGoogle ScholarPubMed
Dong, B, Alpert, P, Zhang, Q, Yu, F (2015) Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides. Oecologia 179:393–403CrossRefGoogle ScholarPubMed
Fan, S, Yu, H, Liu, C, Yu, D, Han, Y, Wang, L (2015) The effects of complete submergence on the morphological and biomass allocation response of the invasive plant Alternanthera philoxeroides. Hydrobiologia 746:159–169CrossRefGoogle Scholar
Fang, ZW, Jiang, WQ, He, YQ, Ma, DF, Liu, YK, Wang, SP, Zhang, YX, Yin, JL (2020) Genome-wide identification, structure characterization, and expression profiling of Dof transcription factor gene family in wheat (Triticum aestivum L.). Agronomy 10:294CrossRefGoogle Scholar
Frandsen, TP, Svensson, B (1998) Plant α-glucosidases of the glycoside hydrolase family 31. Molecular properties, substrate specificity, reaction mechanism, and comparison with family members of different origin. Plant Mol Biol 37:1–13CrossRefGoogle ScholarPubMed
Fung, RWM, Langenkämper, G, Gardner, RC, MacRae, E (2003) Differential expression within an SPS gene family. Plant Sci 164:459–470CrossRefGoogle Scholar
Gao, L, Geng, Y, Yang, H, Hu, Y, Yang, J (2015) Gene expression reaction norms unravel the molecular and cellular processes underpinning the plastic phenotypes of Alternanthera philoxeroides in contrasting hydrological conditions. Front Plant Sci 6:991CrossRefGoogle ScholarPubMed
González-Guzmán, M, Rodríguez, L, Lorenzo-Orts, L, Pons, C, Sarrión-Perdigones, A, Fernández, MA, Peirats-Llobet, M, Forment, J, Moreno-Alvero, M, Cutler, SR, Albert, A, Granell, A, Rodríguez, PL (2014) Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance. J Exp Bot 65:4451–4464CrossRefGoogle ScholarPubMed
Guo, J, Zhou, R, Ren, X, Jia, H, Hua, L, Xu, H, Lv, X, Zhao, J, Wei, T (2018) Effects of salicylic acid, epi-brassinolide and calcium on stress alleviation and Cd accumulation in tomato plants. Ecotox Environ Safe 157:491–496CrossRefGoogle ScholarPubMed
Haas, BJ, Papanicolaou, A, Yassour, M, Grabherr, M, Blood, PD, Bowden, J, Couger, MB, Eccles, D, Li, B, Lieber, M, MacManes, MD, Ott, M, Orvis, J, Pochet, N, Strozzi, Fet al. (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512CrossRefGoogle ScholarPubMed
Hagen, G, Guilfoyle, T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385CrossRefGoogle ScholarPubMed
Iyer, MK, Niknafs, YS, Malik, R, Singhal, U, Sahu, A, Hosono, Y, Barrette, TR, Prensner, JR, Evans, JR, Zhao, S, Poliakov, A, Cao, X, Dhanasekaran, SM, Wu, YM, Robinson, DR, et al. (2015) The landscape of long noncoding RNAs in the human transcriptome. Nature Genet 47:199CrossRefGoogle ScholarPubMed
Li, B, Dewey, CN (2011) RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12:323CrossRefGoogle ScholarPubMed
Li, L, Xu, L, Wang, X, Pan, G, Lu, L (2015) De novo characterization of the alligator weed (Alternanthera philoxeroides) transcriptome illuminates gene expression under potassium deprivation. J Genet 94:95–104CrossRefGoogle ScholarPubMed
Liang, Y, Harris, JM (2005) Response of root branching to abscisic acid is correlated with nodule formation both in legumes and nonlegumes. Am J Bot 92:1675–1683CrossRefGoogle ScholarPubMed
Lin, S, Wu, T, Lin, H, Zhang, Y, Xu, S, Wang, J, Wu, B, Chen, Y, Lin, S, Lin, D, Wang, X, Zhao, X, Wu, J (2018) De novo analysis reveals transcriptomic responses in Eriobotrya japonica fruits during postharvest cold storage. Genes 9:639CrossRefGoogle ScholarPubMed
Liu, D, Horvath, D, Li, P, Liu, W (2019) RNA sequencing characterizes transcriptomes differences in cold response between northern and southern Alternanthera philoxeroides and highlight adaptations associated with northward expansion. Front Plant Sci 10:24CrossRefGoogle ScholarPubMed
Liu, H, Ren, X, Zhu, J, Wu, X, Liang, C (2018) Effect of exogenous abscisic acid on morphology, growth and nutrient uptake of rice (Oryza sativa) roots under simulated acid rain stress. Planta 248:647–659CrossRefGoogle ScholarPubMed
Liu, J, Jung, C, Xu, J, Wang, H, Deng, S, Bernad, L, Arenashuertero, C, Chua, NH (2012) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24:4333–4345CrossRefGoogle ScholarPubMed
Lou, YL, Wang, YQ, Deng, YY, Wei, L (2003) The developmental anatomical study on anomalous in the root and adventitious buds of Altemanthera philoxeroides. Guihaia 24: 125–127. Chinese with English abstractGoogle Scholar
Noguchi, T, Fujioka, S, Takatsuto, S, Sakurai, A, Yoshida, S, Li, JM, Chory, J (1999) Arabidopsis det2 is defective in the conversion of (24R)-24-methylcholest-4-en-3-one to (24R)-24-methyl-5α-cholestan-3-one in brassinosteroid biosynthesis. Plant Physiol 120:833–839CrossRefGoogle ScholarPubMed
Okamura, M, Aoki, N, Hirose, T, Yonekura, M, Ohto, C, Ohsugi, R (2011) Tissue specificity and diurnal change in gene expression of the sucrose phosphate synthase gene family in rice. Plant Sci 181:159–166CrossRefGoogle ScholarPubMed
Park, SY, Fung, P, Nishimura, N, Jensen, DR, Fujii, H, Zhao, Y, Lumba, S, Santiago, J, Rodrigues, A, Chow, TFF, Alfred, SE, Bonetta, D, Finkelstein, R, Provart, NJ, Desveaux, Det al. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1671Google ScholarPubMed
Ravi, V, Chakrabarti, SK, Makeshkumar, T, Saravanan, R (2014) Molecular regulation of storage root formation and development in sweet potato. Pages 157–208 in Janick J, ed. Horticultural Reviews. Volume 42. Hoboken, NJ: WileyCrossRefGoogle Scholar
Ren, H, Gray, WM (2015) SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant 8:1153–1164CrossRefGoogle ScholarPubMed
Rowe, JH, Topping, JF, Liu, J, Lindsey, K (2016) Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin. New Phytol 211:225–239CrossRefGoogle ScholarPubMed
Schnabel, EL, Frugoli, J (2004) The PIN and LAX families of auxin transport genes in Medicago truncatula. Mol Genet Genomics 272:420–432CrossRefGoogle ScholarPubMed
Severing, E, Faino, L, Jamge, S, Busscher, M, Kuijer-Zhang, Y, Bellinazzo, F, Pajoro, A (2018) Arabidopsis thaliana ambient temperature responsive lncRNAs. BMC Plant Boil 18:145CrossRefGoogle ScholarPubMed
Simão, FA, Waterhouse, RM, Ioannidis, P, Kriventseva, EV, Zdobnov, EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212CrossRefGoogle ScholarPubMed
Sojikul, P, Saithong, T, Kalapanulak, S, Pisuttinusart, N, Limsirichaikul, S, Tanaka, M, Utsumi, Y, Sakurai, T, Seki, M, Narangajavana, J (2015) Genome-wide analysis reveals phytohormone action during cassava storage root initiation. Plant Mol Biol 88:531–543CrossRefGoogle ScholarPubMed
Song, Z, Su, Y (2013) Distinctive potassium-accumulation capability of alligatorweed (Alternanthera philoxeroides) links to high-affinity potassium transport facilitated by K+-uptake systems. Weed Sci 61:77–84CrossRefGoogle Scholar
Sturm, A (1995) Development- and organ-specific expression of the genes for sucrose synthase and three isoenzymes of acid β-fructofuranosidase in carrot. Planta 195:601–610CrossRefGoogle Scholar
Sun, J, Zhang, J, Larue, C, Huber, SC (2011) Decrease in leaf sucrose synthesis leads to increased leaf starch turnover and decreased RuBP regeneration-limited photosynthesis but not Rubisco-limited photosynthesis in Arabidopsis null mutants of SPSA1. Plant Cell Environ 34:592–604CrossRefGoogle Scholar
Sun, P, Xiao, X, Duan, L, Guo, Y, Qi, J, Liao, D, Zhao, C, Liu, Y, Zhou, L, Li, X (2015) Dynamic transcriptional profiling provides insights into tuberous root development in Rehmannia glutinosa. Front Plant Sci 6:396CrossRefGoogle ScholarPubMed
Takahashi, F, Sato-Nara, K, Kobayashi, K, Suzuki, M, Suzuki, H (2003) Sugar-induced adventitious roots in Arabidopsis seedlings. J Plant Res 116:83–91CrossRefGoogle ScholarPubMed
Tanaka, M, Kato, N, Nakayama, H, Nakatani, M, Takahata, Y (2008) Expression of class I knotted1-like homeobox genes in the storage roots of sweetpotato (Ipomoea batatas). J Plant Physiol 165:1726–1735CrossRefGoogle Scholar
Tanaka, M, Takahata, Y, Nakatani, M (2005) Analysis of genes developmentally regulated during storage root formation of sweet potato. J Plant Physiol 162:91–102CrossRefGoogle ScholarPubMed
Tsubone, M, Kubota, F, Saitou, K, Kadowaki, M (2000) Enhancement of tuberous root production and adenosine 5′-diphosphate pyrophosphorylase (AGPase) activity in sweet potato (Ipomoea batatas Lam.) by exogenous injection of sucrose solution. J Agron Crop Sci 184:181–186CrossRefGoogle Scholar
Vardhini, BV, Sujatha, E, Rao, SSR (2011) Studies on the effect of brassinosteroids on the qualitative changes in the storage roots of radish. Asian Australas J Biosci Biotechnol 5:27–30Google Scholar
Wang, B, Li, W, Wang, J (2005a) Genetic diversity of Alternanthera philoxeroides in China. Aquat Bot 81:277–283CrossRefGoogle Scholar
Wang, QM, Zhang, ML, Wang, ZL (2005b) Formation and thickening of tuberous roots in relation to the endogenous hormone concentrations in sweet potato. Scientia Agricultura Sinica 38:2414–2420. Chinese with English abstractGoogle Scholar
Xia, Z, Xu, H, Zhai, J, Li, D, Luo, H, He, C, Huang, X (2011) RNA-seq analysis and de novo transcriptome assembly of Hevea brasiliensis. Plant Mol Biol 77:299–308CrossRefGoogle ScholarPubMed
Xu, C, Zhang, W, Fu, C, Lu, B (2003) Genetic diversity of alligator weed in China by RAPD analysis. Biodivers Conserv 12: 637–645CrossRefGoogle Scholar
Yin, JL, Fang, ZW, Sun, C, Zhang, P, Zhang, X, Lu, C, Wang, SP, Ma, DF, Zhu, YX (2018a) Rapid identification of a stripe rust resistant gene in a space-induced wheat mutant using specific locus amplified fragment (SLAF) sequencing. Sci Rep 8:3086CrossRefGoogle Scholar
Yin, JL, Liu, MY, Ma, DF, Wu, JW, Li, SL, Zhu, YX, Han, B (2018b) Identification of circular RNAs and their targets during tomato fruit ripening. Postharvest Biol Technol 136:90–98CrossRefGoogle Scholar
You, W, Han, C, Fang, L, Du, D (2016) Propagule pressure, habitat conditions and clonal integration influence the establishment and growth of an invasive clonal plant, Alternanthera philoxeroides. Front Plant Sci 7:568CrossRefGoogle ScholarPubMed
Yu, J, Hu, SN, Wang, J, Wong, KG, Li, SG, Liu, B, Deng, YJ, Dai, L (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92CrossRefGoogle Scholar
Yuan, J, Zhang, Y, Dong, J, Sun, Y, Lim, BL, Liu, D, Lu, ZJ (2016) Systematic characterization of novel lncRNAs responding to phosphate starvation in Arabidopsis thaliana. BMC Genomics 17:655CrossRefGoogle ScholarPubMed
Yuan, Y, Zhong, M, Shu, S, Du, N, He, L, Yuan, L, Sun, J, Guo, S (2015) Effects of exogenous putrescine on leaf anatomy and carbohydrate metabolism in cucumber (Cucumis sativus L.) under salt stress. J Plant Growth Regul 34:451–464CrossRefGoogle Scholar
Zhou, R, Zhu, YX, Zhao, J, Fang, ZW, Wang, SP, Yin, JL, Chu, ZH, Ma, DF (2018) Transcriptome-wide identification and characterization of potato circular RNAs in response to Pectobacterium carotovorum subspecies brasiliense infection. Int J Mol Sci 19:71CrossRefGoogle Scholar
Zhu, Y, Guo, J, Feng, R, Jia, J, Han, W, Gong, H (2016) The regulatory role of silicon on carbohydrate metabolism in Cucumis sativus L. under salt stress. Plant Soil 406:231–249CrossRefGoogle Scholar
Zhu, Y, Yin, J, Liang, Y, Liu, J, Jia, J, Huo, H, Wu, Z, Yang, R, Gong, H (2019a) Transcriptomic dynamics provide an insight into the mechanism for silicon-mediated alleviation of salt stress in cucumber plants. Ecotox Environ Safe 174:245–254CrossRefGoogle ScholarPubMed
Zhu, YX, Gong, HJ, Yin, JL (2019b) Role of silicon in mediating salt tolerance in plants: a review. Plants 8:147CrossRefGoogle ScholarPubMed
Zhu, YX, Jia, J, Yang, L, Xia, Y, Zhang, H, Jia, J, Zhou, R, Nie, P, Yin, JL, Ma, D, Liu, L (2019c) Identification of cucumber circular RNAs responsive to salt stress. BMC Plant Biol 19:164CrossRefGoogle ScholarPubMed
Zhu, YX, Xu, X, Hu, Y, Han, W, Yin, J, Li, H, Gong, H (2015) Silicon improves salt tolerance by increasing root water uptake in Cucumis sativus L. Plant Cell Rep 34:1629–1646CrossRefGoogle ScholarPubMed
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