Leaf metabolites profiling between red and green phenotypes of Suaeda salsa by widely targeted metabolomics
Xin Wang A , Junhong Bai
A B , Wei Wang A and Guangliang Zhang A
+ Author Affiliations
- Author Affiliations
A State Key Laboratory of Water Environment Simulation, School of Environment, Beijing Normal University, Beijing 100875, China.
B Corresponding author. Email: junhongbai@163.com
Functional Plant Biology 46(9) 845-856 https://doi.org/10.1071/FP18182
Submitted: 9 July 2018 Accepted: 8 May 2019 Published: 3 June 2019
Abstract
The Chenopodiaceae Suaeda salsa (L.) Pall. is a traditional Chinese medicine and food with green and red phenotypes in the Yellow River Delta. We identified 521 metabolites using widely targeted metabolomics, of which 165 were selected as significantly differential metabolites which could be related to the leaf traits of different phenotypes of S. salsa. Two anthocyanins (i.e. cyanidin O-acetylhexoside and delphinidin-3-O-(6ʹ-O-α-rhamnopyranosy l-β-glucopyranoside)) were responsible for red colour in red leaves of S. salsa. Gallic acid, which existed only in red one, was the main reason for leaf succulence. D-arabitol and ribitol were two significantly upregulated carbohydrates in red phenotype. Four alkaloids (i.e. harmaline, aminophylline, pipecolate and trigonelline) were upregulated in red leaves. Hormonal changed involved a decrease in indoleacetic acid-valine (IAA-Val), N6-isopentenyladenosine-5ʹ-monophosphate (iPRMP), isopentenyladenineriboside (iPR), trans-abscisic acid (S-ABA), salicylic acid O-hexoside, methyl jasmonate, N6-isopentenyladenine (iP), trans-zeatin riboside-O-glucoside iso2, trans-zeatin riboside-O-glucoside, and a tendency for dihydrozeatin 9-O-glucoside (DZ9G) down accumulation. In addition, the regulation of amino acids and lipids also contributed to the adaptation of red phenotype to harsh environment. Generally, our findings provide a comprehensive comparison of the metabolites between two phenotypes of S. salsa and an interpretation of phenotypic differences from the point of metabolomics.
Additional keywords: alkaloid, anthocyanin, flavonoid, hormone, metabolomics, Suaeda salsa.
References
Bai JH, Wang X, Jia J, Zhang GL, Wang YY, Zhang S (2017) Denitrification of soil nitrogen in coastal and inland salt marshes with different flooding frequencies. Physics and Chemistry of the Earth 97, 31–36.| Denitrification of soil nitrogen in coastal and inland salt marshes with different flooding frequencies.Crossref | GoogleScholarGoogle Scholar |
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Critical Reviews in Plant Sciences 24, 23–58.
| Drought and salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Behl RK, Moawad AM, Achtnich W (1991) Amino acid and protein profile changes in a spring wheat mutant under prolonged heat stress. Annals of Biology 7, 63–68.
Birt DF, Jeffery E (2013) Flavonoids. Advances in Nutrition 4, 576–577.
| Flavonoids.Crossref | GoogleScholarGoogle Scholar | 24038263PubMed |
Boriboonkaset T, Theerawitaya C, Yamada N, Pichakum A, Supaibulwatana K, Cha-Um S, Takabe T, Kirdmanee C (2013) Regulation of some carbohydrate metabolism-related genes, starch and soluble sugar contents, photosynthetic activities and yield attributes of two contrasting rice genotypes subjected to salt stress. Protoplasma 250, 1157–1167.
| Regulation of some carbohydrate metabolism-related genes, starch and soluble sugar contents, photosynthetic activities and yield attributes of two contrasting rice genotypes subjected to salt stress.Crossref | GoogleScholarGoogle Scholar | 23558902PubMed |
Cha-um S, Charoenpanich A, Roytrakul S, Kirdmanee C (2009) Sugar accumulation, photosynthesis and growth of two indica rice varieties in response to salt stress. Acta Physiologiae Plantarum 31, 477–486.
| Sugar accumulation, photosynthesis and growth of two indica rice varieties in response to salt stress.Crossref | GoogleScholarGoogle Scholar |
Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu X, Yu S, Xiong L, Luo J (2013) A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Molecular Plant 6, 1769–1780.
| A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics.Crossref | GoogleScholarGoogle Scholar | 23702596PubMed |
Chen Q, Lu XY, Guo XR, Guo QX, Li DW (2017) Metabolomics characterization of two Apocynaceae plants, Catharanthus roseus and Vinca minor, using GC-MS and LC-MS methods in combination. Molecules (Basel, Switzerland) 22, 997
| Metabolomics characterization of two Apocynaceae plants, Catharanthus roseus and Vinca minor, using GC-MS and LC-MS methods in combination.Crossref | GoogleScholarGoogle Scholar |
Corcoran MP, McKay DL, Blumberg JB (2012) Flavonoid basics: chemistry, sources, mechanisms of action, and safety. Journal of Nutrition in Gerontology and Geriatrics 31, 176–189.
| Flavonoid basics: chemistry, sources, mechanisms of action, and safety.Crossref | GoogleScholarGoogle Scholar | 22888837PubMed |
Davis B (2005) Growing pains for metabolomics. Scientist (Philadelphia, Pa.) 19, 25–28.
Ding HR, Hong LZ, Yang ZQ, Wang MW, Wang K, Zhu XW (2008) Progress of study on halophyte Suaeda salsa. Jiangxi Nongye Daxue Xuebao 20, 35–37. [In Chinese]
Dong X, Chen W, Wang W, Zhang H, Liu X, Luo J (2014) Comprehensive profiling and natural variation of flavonoids in rice. Journal of Integrative Plant Biology 56, 876–886.
| Comprehensive profiling and natural variation of flavonoids in rice.Crossref | GoogleScholarGoogle Scholar | 24730595PubMed |
Dubey RS, Singh AK (1999) Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolizing enzymes in rice plants. Biologia Plantarum 42, 233–239.
| Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolizing enzymes in rice plants.Crossref | GoogleScholarGoogle Scholar |
Fernie AR, Schauer N (2009) Metabolomics-assisted breeding: a viable option for crop improvement? Trends in Genetics 25, 39–48.
| Metabolomics-assisted breeding: a viable option for crop improvement?Crossref | GoogleScholarGoogle Scholar | 19027981PubMed |
Fukushima A, Nakamura M, Suzuki H, Yamazaki M, Knoch E, Mori T, Umemoto N, Morita M, Hirai G, Sodeoka M, Saito K (2016) Comparative characterization of the leaf tissue of Physalis alkekengi and Physalis peruviana using RNA-seq and metabolite profiling. Frontiers in Plant Science 7, 1883
| Comparative characterization of the leaf tissue of Physalis alkekengi and Physalis peruviana using RNA-seq and metabolite profiling.Crossref | GoogleScholarGoogle Scholar | 28066454PubMed |
Getachew G, Pittroff W, Putnam DH, Dandekar A, Goyal S, Depeters EJ (2008) The influence of addition of gallic acid, tannic acid, or quebracho tannins to alfalfa hay on in vitro rumen fermentation and microbial protein synthesis. Animal Feed Science and Technology 140, 444–461.
| The influence of addition of gallic acid, tannic acid, or quebracho tannins to alfalfa hay on in vitro rumen fermentation and microbial protein synthesis.Crossref | GoogleScholarGoogle Scholar |
Gilbert GA, Gadush MV, Wilson C, Madore MA (1998) Amino acid accumulation in sink and source tissues of Coleus blumei Benth. during salinity stress. Journal of Experimental Botany 49, 107–114.
| Amino acid accumulation in sink and source tissues of Coleus blumei Benth. during salinity stress.Crossref | GoogleScholarGoogle Scholar |
Goddard NJ, Dunn MA, Zhang L, White AJ, Jack PL, Hughes MA (1993) Molecular analysis and spatial expression pattern of a low-temperature-specific barley gene, BLT 101. Plant Molecular Biology 23, 871–879.
| Molecular analysis and spatial expression pattern of a low-temperature-specific barley gene, BLT 101.Crossref | GoogleScholarGoogle Scholar | 8251639PubMed |
Griffin JL (2006) Understanding mouse models of disease through metabolomics. Current Opinion in Chemical Biology 10, 309–315.
| Understanding mouse models of disease through metabolomics.Crossref | GoogleScholarGoogle Scholar | 16815732PubMed |
Janz D, Behnke K, Schnitzler JP, Kanawati B, Schmitt-Kopplin P, Polle A (2010) Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms BMC Plant Biology 10, 150
| Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanismsCrossref | GoogleScholarGoogle Scholar | 20637123PubMed |
Joshi V, Joung JQ, Fei ZJ, Jander G (2010) Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids 39, 933–947.
| Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress.Crossref | GoogleScholarGoogle Scholar | 20186554PubMed |
Kalamaki MS, Merkouropoulos G, Kanellis AK (2009) Can ornithine accumulation modulate abiotic stress tolerance in Arabidopsis? Plant Signaling & Behavior 4, 1099–1101.
| Can ornithine accumulation modulate abiotic stress tolerance in Arabidopsis?Crossref | GoogleScholarGoogle Scholar |
Kanehisa M, Goto S, Kawashima S, Nakaya A (2002) The KEGG databases at GenomeNet Nucleic Acids Research 30, 42–46.
| The KEGG databases at GenomeNetCrossref | GoogleScholarGoogle Scholar | 11752249PubMed |
Kaplan F, Guy CL (2004) β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiology 135, 1674–1684.
| β-Amylase induction and the protective role of maltose during temperature shock.Crossref | GoogleScholarGoogle Scholar | 15247404PubMed |
Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings Crop Science 40, 482
| Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlingsCrossref | GoogleScholarGoogle Scholar |
Kettunen J, Tukiainen T, Sarin AP, Ortega-Alonso A, Tikkanen E, Lyytikäinen L, Kangas AJ, Soininen P, Würtz P, Silander K, et al (2012) Genome-wide association study identifies multiple loci influencing human serum metabolite levels. Nature Genetics 44, 269–276.
| Genome-wide association study identifies multiple loci influencing human serum metabolite levels.Crossref | GoogleScholarGoogle Scholar | 22286219PubMed |
Khan MIR, Fatma M, Pe TS, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Frontiers in Plant Science 6, 462
| Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants.Crossref | GoogleScholarGoogle Scholar |
Koes RE, Quattrocchio F, Mol JNM (1994) The flavonoid biosynthetic pathway in plants: Function and evolution. BioEssays 16, 123–132.
| The flavonoid biosynthetic pathway in plants: Function and evolution.Crossref | GoogleScholarGoogle Scholar |
Kohorn BD, Kohorn SL (2012) The cell wall-associated kinases, WAKs, as pectin receptors. Frontiers in Plant Science 3, 88
| The cell wall-associated kinases, WAKs, as pectin receptors.Crossref | GoogleScholarGoogle Scholar | 22639672PubMed |
Kumar A, Naik GK, Simmi PS, Giridhar P (2015) Salinity and drought response alleviate caffeine content of young leaves of Coffea canephora var. Robusta cv. S274. Journal of Applied Biology and Biotechnology 3, 50–60.
Lee SJ, Jeong EM, Ki AY, Oh KS, Kwon J, Jeong JH, Chung NJ (2016) Oxidative defense metabolites induced by salinity stress in roots of Salicornia herbacea. Journal of Plant Physiology 206, 133–142.
| Oxidative defense metabolites induced by salinity stress in roots of Salicornia herbacea.Crossref | GoogleScholarGoogle Scholar | 27770750PubMed |
Li Y, Zhang YZ, Guo L, Wang Y, Wang XH (2015) Study on extraction and antioxidant activity of flavonoids from heteroptera saline seepweed. Food Research and Development 36, 38–41.
Liu T, Staden VJ (2001) Partitioning of carbohydrates in salt-sensitive and salt-tolerant soybean callus cultures under salinity stress and its subsequent relief. Plant Growth Regulation 33, 13–17.
| Partitioning of carbohydrates in salt-sensitive and salt-tolerant soybean callus cultures under salinity stress and its subsequent relief.Crossref | GoogleScholarGoogle Scholar |
Liu Y, Ding TL, Wang BS (2006) Study on the leaf succulence of Suaeda salsa under differently natural saline environments. Journal of Shandong Normal University 21, 102–104. [In Chinese]
Lunn JE, Delorge I, Figueroa CM, Dijck VP, Stitt M (2014) Trehalose metabolism in plants. The Plant Journal 79, 544–567.
| Trehalose metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 24645920PubMed |
Matsuda F, Okazaki Y, Oikawa A, Kusano M, Nakabayashi R, Kikuchi J, Yonemaru J, Ebana K, Yano M, Saito K (2012) Dissection of genotype-phenotype associations in rice grains using metabolome quantitative trait loci analysis. The Plant Journal 70, 624–636.
| Dissection of genotype-phenotype associations in rice grains using metabolome quantitative trait loci analysis.Crossref | GoogleScholarGoogle Scholar | 22229385PubMed |
Panche AN, Diwan AD, Chandra SR (2016) Flavonoids: an overview. Journal of Nutritional Science 5, e47
| Flavonoids: an overview.Crossref | GoogleScholarGoogle Scholar | 28620474PubMed |
Rasool S, Ahmad A, Siddiqi TO, Ahmad P (2013) Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress. Acta Physiologiae Plantarum 35, 1039–1050.
| Changes in growth, lipid peroxidation and some key antioxidant enzymes in chickpea genotypes under salt stress.Crossref | GoogleScholarGoogle Scholar |
Richter JA, Erban A, Kopka J, Zörb C (2015) Metabolic contribution to salt stress in two maize hybrids with contrasting resistance. Plant Science 233, 107–115.
| Metabolic contribution to salt stress in two maize hybrids with contrasting resistance.Crossref | GoogleScholarGoogle Scholar | 25711818PubMed |
Rose JKC, Lee SJ (2010) Straying off the highway: trafficking of secreted plant proteins and complexity in the plant cell wall proteome. Plant Physiology 153, 433–436.
| Straying off the highway: trafficking of secreted plant proteins and complexity in the plant cell wall proteome.Crossref | GoogleScholarGoogle Scholar |
Ryan KG, Swinny EE, Markham KR, Winefield C (2002) Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves. Phytochemistry 59, 23–32.
| Flavonoid gene expression and UV photoprotection in transgenic and mutant Petunia leaves.Crossref | GoogleScholarGoogle Scholar | 11754940PubMed |
Ryu HJ, Cho YG (2015) Plant hormones in salt stress tolerance. Journal of Plant Biology 58, 147–155.
| Plant hormones in salt stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Sadowsky A, Mettler-Altmann T, Ott S (2016) Metabolic response to desiccation stress in strains of green algal photobionts (Trebouxia) from two Antarctic lichens of southern habitats. Phycologia 55, 703–714.
| Metabolic response to desiccation stress in strains of green algal photobionts (Trebouxia) from two Antarctic lichens of southern habitats.Crossref | GoogleScholarGoogle Scholar |
Shao HM, Sun SQ, Xu HJ (1996) The determination of seven water-soluble vitamins and eighteen amino acids in Suaeda salsa (L.) Pall. juice by high performance liquid chromatography. Se Pu 14, 235 . [In Chinese]
Tattini M, Gucci R, Romani A, Baldi A, Everard JD (1996) Changes in non-structural carbohydrates in olive (Olea europaea) leaves during root zone salinity stress. Physiologia Plantarum 98, 117–124.
| Changes in non-structural carbohydrates in olive (Olea europaea) leaves during root zone salinity stress.Crossref | GoogleScholarGoogle Scholar |
Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma S (2017) Abscisic acid signalling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Frontiers in Plant Science 8, 161
| Abscisic acid signalling and abiotic stress tolerance in plants: a review on current knowledge and future prospects.Crossref | GoogleScholarGoogle Scholar | 28265276PubMed |
Wang ZJ (2009) Studies on separation purification and antioxidant activity of a water-soluble polysaccharide SPA from Suaeda spp. Journal of Liaoning University of TCM 11, 168–169. [In Chinese]
Wang L (2014) Study on functional constituents of Suaeda. Masters thesis. Dalian Polytechnic University, Liaoning, China.
Wang CQ, Zhao JQ, Chen M, Wang BS (2006) Identification of betacyanin and effects of environmental factors on its accumulation in halophyte Suaeda salsa. Journal of Plant Physiology and Molecular Biology 32, 195–201. [In Chinese]
Wang L, Yue XX, Wang BS (2008) The comparative study on POD in the leaves of two different phenotypes of Suaeda salsa L. grown under different natural conditons. Journal of Shandong Normal University 23, 103–105. [In Chinese]
Wang Q, Xiu YW, Wang BS (2010) Comparison of leaf pigments between two phenotypes of Suaeda salsa L. seedlings under NaCl stress. Journal of Shandong Normal University 25, 130–140. [In Chinese]
Wei CF, Cui YY, Zhou FQ (2016) Morphology and structure of two phenotypes of Suaeda salsa in different habitats. Chinese Journal of Marine Drugs 3, 57–61. [In Chinese]
Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiology 126, 485–493.
| Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology.Crossref | GoogleScholarGoogle Scholar | 11402179PubMed |
Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5, 218–223.
| Biosynthesis of flavonoids and effects of stress.Crossref | GoogleScholarGoogle Scholar | 11960739PubMed |
Xie T, Cui BS, Bai JH, Li SZ, Zhang SY (2018) Rethinking the role of edaphic condition in halophyte vegetation degradation on salt marshes due to coastal defense structure. Physics and Chemistry of the Earth 103, 81–90.
| Rethinking the role of edaphic condition in halophyte vegetation degradation on salt marshes due to coastal defense structure.Crossref | GoogleScholarGoogle Scholar |
Xu HJ (2006) Determination of 9 trace elements in Suaeda salsa. Chinese Journal of Pest Control 22, 459 . [In Chinese]
Xu HJ (2008) Determination of 18 Amino Acids in Suaeda salsa. Chinese Journal of Pest Control 24, 161 . [In Chinese]
Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M, Lunn JE (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. Journal of Experimental Botany 65, 1051–1068.
| The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P.Crossref | GoogleScholarGoogle Scholar | 24420566PubMed |
Yue XX, Chen M, Duan D, Wang BS (2008) Comparative study on antioxidant system of green and red-violet phenotype Suaeda salsa leaves. Journal of Shangdong Normal University 23, 121–124. [In Chinese]
Zhang XJ, Fan SJ, Li FZ (2003) Development and utilization of Suaeda salsa in China. Chinese Wild Plant Resources 22, 1–3. [In Chinese]
Zhang JY, Li MH, Xu LM, Wang ZJ (2008) Effect of Suaeda seed oil on blood-fat and immunologic function of mouse. Occupational Health 24, 1529–1530. [In Chinese]
Zhang A, Fang Y, Wang H, Li H, Zhang Z (2011a) Free-radical scavenging properties and reducing power of grape cane extracts from 11 selected grape cultivars widely grown in China. Molecules (Basel, Switzerland) 16, 10104–10122.
| Free-radical scavenging properties and reducing power of grape cane extracts from 11 selected grape cultivars widely grown in China.Crossref | GoogleScholarGoogle Scholar |
Zhang XX, Li CJ, Nan ZB (2011b) Effects of salt and drought stress on alkaloid production in endophyte-infected drunken horse grass (Achnatherum inebrians). Biochemical Systematics and Ecology 39, 471–476.
| Effects of salt and drought stress on alkaloid production in endophyte-infected drunken horse grass (Achnatherum inebrians).Crossref | GoogleScholarGoogle Scholar |
