Metabolomics Analysis of Lagerstroemia indica in Response to Salt and Alkali Stress

doi:10.7525/j.issn.1673-5102.2024.03.011

Abstract

Abstract:

To explore the metabolic response mechanism of Lagerstroemia indica ‘Pink Velour’ to salt and alkali stresses， one-year-old asexual cottage seedlings were treated to salt stress（NaCl， pH=7.02） and alkali stress（NaHCO₃ and Na₂CO₃， Na⁺ mole ratio 2∶1， pH=9.52） respectively， and the leaves metabolic changes and differences of the two treatment groups and the control group（CK） were analyzed and compared by using liquid chromatography mass spectrometry（LC-MS）. The results showed that 156 and 176 different metabolites were screened in salt and alkali stress group respectively， and 23 different metabolites were screened in both groups， and the rest were unique different metabolites. KEGG enrichment analysis showed that the biosynthesis of secondary metabolites， amino acid metabolism， carbohydrate metabolism， fatty acid metabolism and plant hormone synthesis were main metabolic pathways in response to salt and alkali stress. Glycine， serine and threonine anabolism， ABC transporter protein and Vitamin B₆ anabolism were the unique metabolic pathways in salt stress groups. Biosynthesis of valine， leucine， isoleucine， arginine， proline， folic acid and ascorbic acid， and mutual transformation between pentose and glucuronic were the unique metabolic pathway in alkali stress groups. The changes of different metabolites and enriched metabolic pathways might be the main mechanism of L. indica response to the salt stress and alkali stress.

Key words: Lagerstroemia indica, metabolomics, salt stress, alkali stress

CLC Number:

Q718.43

Hengfeng ZHANG, Yangwu HE, Huanchao ZHANG, Qingcui WEI. Metabolomics Analysis of Lagerstroemia indica in Response to Salt and Alkali Stress[J]. Bulletin of Botanical Research, 2024, 44(3): 420-430.

Figures/Tables 9

Fig.1

Fig.2

Fig.3

Fig.4

Fig.5

Table 1

Fig.6

Table 2

Fig.7

References 28

1	杨劲松，姚荣江，王相平，等.中国盐渍土研究：历程、现状与展望［J］.土壤学报，2022，59（1）：10-27.
	YANG J S， YAO R J， WANG X P，et al.Research on salt-affected soils in China：history，status quo and prospect［J］.Acta Pedologica Sinica，2022，59（1）：10-27.
2	李晓院，解莉楠.盐胁迫下植物Na⁺调节机制的研究进展［J］.生物技术通报，2019，35（7）：148-155.
	LI X Y， XIE L N.Research progress in Na⁺ regulation mechanism of plants under salt stress［J］.Biotechnology Bulletin，2019，35（7）：148-155.
3	李焕勇，杨秀艳，唐晓倩，等.植物响应盐胁迫组学研究进展［J］.西北植物学报，2016，36（12）：2548-2557.
	LI H Y， YANG X Y， TANG X Q，et al.Omics research progress of plants under salt stress［J］.Acta Botanica Boreali-Occidentalia Sinica，2016，36（12）：2548-2557.
4	方文培，张泽荣.中国植物志：第52卷：第2分册［M］.北京：科学出版社，1983：94.
	FANG W P， ZHANG Z R.Flora of China：Vol.52：Series 2［M］.Beijing：Scinece Press，1983：94.
5	贾永正，张子晗，俞方圆，等.盐胁迫对紫薇种子萌发特性的影响［J］.种子，2016，35（10）：87-91.
	JIA Y Z， ZHANG Z H， YU F Y，et al.Effects of salt stress on germination characteristics of Lagerstroemia indica seeds［J］.Seed，2016，35（10）：87-91.
6	邱国金，胡卫霞，孙其松，等.盐胁迫对紫薇3个新品种的生长与生理特性的影响［J］.西部林业科学，2017，46（4）：50-55.
	QIU G J， HU W X， SUN Q S，et al.Salt stress effect on the growth and physiological characteristics of three new varieties of Lagerstroemia indica ［J］.Journal of West China Forestry Science，2017，46（4）：50-55.
7	邱国金，于敏，胡卫霞，等.盐胁迫对天鹅绒紫薇生长与生理生化特性的影响［J］.江苏农业科学，2018，46（6）：123-126.
	QIU G J， YU M， HU W X，et al.Salt stress effect on the growth and physiological-biochemical characteristics of Lagerstroemia indica ‘Pink Velour’［J］.Jiangsu Agricultural Sciences，2018，46（6）：123-126.
8	FIEHN O.Metabolomics-the link between genotypes and phenotypes［J］.Plant Molecular Biology，2002，48（2）：155-171.
9	YE T T， SHI H T， WANG Y P，et al.Contrasting proteomic and metabolomic responses of bermudagrass to drought and salt stresses［J］.Frontiers in Plant Science，2016，7：1694-1709.
10	高龙飞，贾斌，张卫华，等.盐胁迫下蓝莓叶片生理特性与代谢组学分析［J］.植物生理学报，2022，58（1）：155-164.
	GAO L F， JIA B， ZHANG W H，et al.Physiological characteristics and metabonomics analysis of blueberry leaves under salt stress［J］.Plant Physiology Journal，2022，58（1）：155-164.
11	闫海冰，张慧芳，冯帆，等.2种白刺对盐胁迫的代谢响应机制［J］.林业科学，2021，57（1）：20-29.
	YAN H B， ZHANG H F， FENG F，et al.Metabolic response mechanism of two Nitraria species to salt stress［J］.Scientia Silvae Sinicae，2021，57（1）：20-29.
12	付海奇，刘晓，宋姝，等.次生代谢物调控植物抵抗盐碱胁迫的机制［J］.植物生理学报，2023，59（4）：727-740.
	FU H Q， LIU X， SONG S，et al.Mechanisms of secondary metabolites regulating plant resistance to salinity and alkali stress［J］.Plant Physiology Journal，2023，59（4）：727-740.
13	LLANES A， BERTAZZA G， PALACIO G，et al.Different sodium salts cause different solute accumulation in the halophyte Prosopis strombulifera ［J］.Plant Biology，2013，15（s1）：118-125.
14	李娜娜，刘同歌，黄志慧，等.草本资源植物菥蓂对盐胁迫下生理生态及次生代谢产物响应［J］.草业学报，2022，31（11）：181-190.
	LI N N， LIU T G， HUANG Z H，et al.Physiological ecological and secondary metabolic responses of the herbaceous resource plant Thlaspi arvense to salt stress［J］.Acta Prataculturae Sinica，2022，31（11）：181-190.
15	邢芳芳，高明夫，周传志，等.氨基酸与植物抗逆性关系的研究进展［J］.黑龙江农业科学，2018，41（3）：150-155.
	XING F F， GAO M F， ZHOU C Z，et al.Advances in the relationship between amino acid and plant stress resistance［J］.Heilongjiang Agricultural Sciences，2018，41（3）：150-155.
16	燕辉，彭晓邦，薛建杰.NaCl胁迫对花棒叶片光合特性及游离氨基酸代谢的影响［J］.应用生态学报，2012，23（7）：1790-1796.
	YAN H， PENG X B， XUE J J.Effects of NaCl stress on leaf photosynthesis characteristics and free amino acid metabolism of Heyedysarum scoparium ［J］.Chinese Journal of Applied Ecology，2012，23（7）：1790-1796.
17	RICHTER J A， ERBAN A， KOPKA J，et al.Metabolic contribution to salt stress in two maize hybrids with contrasting resistance［J］.Plant Science，2015，233：107-115.
18	LI X N， HAN S J， WANG G Y，et al.The fungus Aspergillus aculeatus enhances salt-stress tolerance，metabolite accumulation，and improves forage quality in perennial ryegrass［J］.Frontiers in Microbiology，2017，8：1664.
19	刘文献，刘志鹏，谢文刚，等.脂肪酸及其衍生物对植物逆境胁迫的响应［J］.草业科学，2014，31（8）：1556-1565.
	LIU W X， LIU Z P， XIE W G，et al.Responses of fatty acid and its derivatives to stress in plants［J］.Pratacultural Science，2014，31（8）：1556-1565.
20	YANG D S， ZHANG J， LI M X，et al.Metabolomics analysis reveals the salt-tolerant mechanism in Glycine soja ［J］.Journal of Plant Growth Regulation，2017，36（2）：460-471.
21	蔡美杰，张恩慧，张鑫鑫，等.盐胁迫甘蓝DH幼苗添加细胞分裂素效果研究［J］.东北农业大学学报，2019，50（5）：19-25.
	CAI M J， ZHANG E H， ZHANG X X，et al.Study on adding cytokinin to DH seedlings of cabbage under salt stress［J］.Journal of Northeast Agricultural University，2019，50（5）：19-25.
22	李昕儒，高宇，苗淑楠，等.油莎豆生长素受体TIR1基因家族鉴定及响应盐胁迫和外源IBA的表达分析［J］.热带作物学报，2023，44（5）：894-904.
	LI X R， GAO Y， MIAO S N，et al.Identification of auxin receptor gene TIR1 family in Cyperus esculentus and the expression analysis in response to salt stress and exogenous IBA［J］.Chinese Journal of Tropical Crops，2023，44（5）：894-904.
23	张衡锋，杨绮，韦庆翠，等.盐胁迫对10个品种紫薇的影响及其耐盐性综合评价［J］.东北林业大学学报，2023，51（9）：34-40.
	ZHANG H F， YANG Q， WEI Q C，et al.Effects of salt stress and salt tolerance on ten Lagerstroemia indica varieties［J］.Journal of Northeast Forestry University，2023，51（9）：34-40.
24	DIÉDHIOU C J， POPOVA O V， DIETZ K J，et al.The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice［J］.BMC Plant Biology，2008，8（1）：49.
25	黄龙全，张剑韵.植物维生素B₆从头合成与代谢转换研究进展［J］.西北植物学报，2015，35（10）：2124-2131.
	HUANG L Q， ZHANG J Y.Review on the de novo synthesis and metabolic conversions of vitamin B₆ in plants［J］.Acta Botanica Boreali-Occidentalia Sinica，2015，35（10）：2124-2131.
26	李焕勇，杨秀艳，唐晓倩，等.盐胁迫下西伯利亚白刺根代谢组学分析［J］.植物生理学报，2020，56（7）：1617-1626.
	LI H Y， YANG X Y， TANG X Q，et al.Metabolomics analysis of Nitraria sibirica roots under salt stress［J］.Plant Physiology Journal，2020，56（7）：1617-1626.
27	李莎，姜凌，王崇英，等.叶酸在植物体内功能的研究进展［J］.植物学报，2012，47（5）：525-533.
	LI S， JIANG L， WANG C Y，et al.Research advances in the functions of plant folates［J］.Chinese Bulletin of Botany，2012，47（5）：525-533.
28	PERIN E C， SILVA MESSIAS RDA， BOROWSKI J M，et al.ABA-dependent salt and drought stress improve strawberry fruit quality［J］.Food Chemistry，2019，271：516-526.

代谢物类型 Metabolite type	A vs C		B vs C
代谢物类型 Metabolite type	上调Up	下调Down	上调Up	下调Down
汇总Total	66	90	75	101
生物碱及衍生物Alkaloids and derivatives	1	1	0	0
苯环型化合物Benzenoids	7	5	5	11
木脂素、新木脂素及相关化合物Lignans，neolignans and related compounds	0	0	2	1
脂质和类脂分子Lipids and lipid-like molecules	11	19	20	27
核苷、核苷酸和类似物Nucleosides，nucleotides， and analogues	7	5	3	1
有机酸及其衍生物Organic acids and derivatives	7	7	7	9
有机氮化合物Organic nitrogen compounds	0	3	3	2
有机氧化合物Organic oxygen compounds	11	15	12	24
有机杂环化合物Organic heterocyclic compounds	13	15	3	11
苯丙类和聚酮类Phenylpropanoids and polyketides	6	15	14	10
其他Others	3	5	6	5

类别 Category	差异代谢物数量 Differential metabolites number
类别 Category	A vs C	B vs C
总计Total	62	48
次生代谢产物生物合成Biosynthesis of secondary metabolites	15	10
氨基酸代谢Amino acid metabolism	10	10
脂质代谢Lipid metabolism	9	5
核苷酸代谢Nucleotide metabolism	7	5
萜类和多酮类代谢Metabolism of terpenoids and polyketides	6	5
膜转运Membrane transport	5	0
碳水化合物代谢Carbohydrate metabolism	3	4
信号传导Signal transduction	2	0
其他氨基酸代谢Metabolism of other amino acids	2	3
翻译Translation	1	2
能量代谢Energy metabolism	1	0
辅助因子和维生素代谢Metabolism of cofactors and vitamins	1	4

[1]	Chenxi MA, Yu ZHANG, Dexin KONG, Ying GAO, Lijian XU, Wei MENG. Analysis of Fungi from Parametarhizium on Improving the Growth of Mung Beans under Salt and Alkali Stress [J]. Bulletin of Botanical Research, 2024, 44(2): 239-247.
[2]	Fazhi FANG, Huiying GUI, Zhaojia LI, Xiaofeng ZHANG. Physiological Adaptation of Six Mangrove Seedlings to Different Salinity [J]. Bulletin of Botanical Research, 2023, 43(6): 881-889.
[3]	Shuyao ZHUANG, Hengbo XU, Xiaoyu HU, Shang DAI, Yanni ZHANG. Effects of Saline-alkali Stress on Growth and Physiological Characteristics of Color Leaf Heuchera micrantha ‘Silver Fan’ Seedlings [J]. Bulletin of Botanical Research, 2023, 43(4): 520-530.
[4]	Lei XU, Xiao XU, Qinsong LIU. Effects of Exogenous Salicylic Acid on Antioxidant System and Gene Expression of Davidia involucrata Seedlings under Salt Stress [J]. Bulletin of Botanical Research, 2023, 43(4): 572-581.
[5]	Li LI, Xin WANG, Yuejing ZHANG, Lingyun JIA, Hailong PANG, Hanqing FENG. Effects of Abiotic Stresses on the Intracellular and Extracellular ATP Levels of Tobacco Suspension Cells [J]. Bulletin of Botanical Research, 2023, 43(2): 179-185.
[6]	Shixian LIAO, Yuting WANG, Liben DONG, Yongmei GU, Fenglin JIA, Tingbo JIANG, Boru ZHOU. Function Analysis of the Transcription Factor PsnbZIP1 of Populus simonii×P. nigra in Response to Salt Stress [J]. Bulletin of Botanical Research, 2023, 43(2): 288-299.
[7]	Senyao LIU, Fenglin JIA, Qing GUO, Gaofeng FAN, Boru ZHOU, Tingbo JIANG. Response Analysis of Transcription Factor PsnbHLH162 Gene in Populus simonii × P. nigra under Salt Stress and Low Temperature Stress [J]. Bulletin of Botanical Research, 2023, 43(2): 300-310.
[8]	Jianxin LIU, Ruirui LIU, Xiuli LIU, Xiaobin OU, Haiyan JIA, Ting BU, Na LI. Effects of Exogenous Hydrogen Sulfide on Contents of Organic Acids and Hormones in Leaves of Avena nuda under Saline-Alkali Stress [J]. Bulletin of Botanical Research, 2023, 43(1): 76-89.
[9]	Yan WU, Sai LI, Kexin WU, Liqiang MU. Differences in Leaf Metabolism of Wild Rosa acicularis and Rosa acicularis ‘Luhe’ Based on GC-MS [J]. Bulletin of Botanical Research, 2022, 42(6): 1070-1078.
[10]	Liran YUE, Yingjie LIU, Chenxu LIU, Yunwei ZHOU. Cloning and Functional Analysis of miR398a from Chrysanthemum× grandiflora in Response to Salt Stress [J]. Bulletin of Botanical Research, 2022, 42(6): 986-996.
[11]	Denggao LI, Rui LIN, Qinghui MU, Na ZHOU, Yanru ZHANG, Wei BAI. Cloning and Functional Analysis of StNPR4 gene in Solanum tuberosum [J]. Bulletin of Botanical Research, 2022, 42(5): 821-829.
[12]	Liben PAN, Xue YAN, Jia LIU, Kexin WU, Yang LIU, Shaochong LIU. Physiological Characteristics of Early Spring Flowering Plants under Northeast Forest [J]. Bulletin of Botanical Research, 2022, 42(4): 657-666.
[13]	Jiaorao CHEN, Xu XU, Zhangli HU, Shuang YANG. Recent Advances on Salt Stress Sensitivity and Related Calcium Signals in Plants [J]. Bulletin of Botanical Research, 2022, 42(4): 713-720.
[14]	He CHENG, Shuanghui TIAN, Yang ZHANG, Cong LIU, De’an XIA, Zhigang WEI. Genome-wide Identification and Expression Analysis of nsLTP Gene Family in Populus trichocarpa [J]. Bulletin of Botanical Research, 2022, 42(3): 412-423.
[15]	Jianxin LIU, Ruirui LIU, Xiuli LIU, Haiyan JIA, Ting BU, Na LI. Effects of Spraying NaHS at Different Growth Stages on H₂S Production and Reactive Oxygen Species Metabolism of Naked Oat Leaves under Saline-Alkali Stress [J]. Bulletin of Botanical Research, 2022, 42(3): 455-465.