Cold stress increases salt tolerance of the extremophytes Eutrema salsugineum (Thellungiella salsuginea) and Eutrema (Thellungiella) botschantzevii

Salinity strongly impairs plant growth and development. Natural genetic variation can be used to dissect complex traits such as plant salt tolerance. We used 16 accessions of the halophytic species Eutrema salsugineum (previously called Thellungiella salsuginea (Pallas) O.E.Schulz, Thellungiella halophila (C.A.Meyer) O.E. Schulz and Thellungiella botschantzevii D.A.German to investigate their natural variation in salinity tolerance. Although all accessions showed survival and growth up to 700 mM NaCl in hydroponic culture, their relative salt tolerance varied considerably. All accessions accumulated the compatible solutes proline, sucrose, glucose and fructose and the polyamines putrescine and spermine. Relative salt tolerance was not correlated with the content of any of the investigated solutes. We compared the metabolomes and transcriptomes of Arabidopsis thaliana (L. Heynh.) Col-0 and E. salsugineum Yukon under control and salt stress conditions. Higher content of several metabolites in Yukon compared with Col-0 under control conditions indicated metabolic pre-adaptation to salinity in the halophyte. Most metabolic salt responses in Yukon took place at 200 mM NaCl, whereas few additional changes were observed between 200 and 500 mM. The opposite trend was observed for the transcriptome, with only little overlap between salt-regulated genes in the two species. In addition, only about half of the salt-regulated Yukon unigenes had orthologues in Col-0.

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Ectopic expression of a LEA protein gene TsLEA1 from Thellungiella salsuginea confers salt-tolerance in yeast and Arabidopsis

Molecular Biology Reports ◽

10.1007/s11033-011-1254-8 ◽

2011 ◽

Vol 39 (4) ◽

pp. 4627-4633 ◽

Cited By ~ 17

Author(s):

Yiyue Zhang ◽

Yin Li ◽

Jianbin Lai ◽

Huawei Zhang ◽

Yuanyuan Liu ◽

...

Keyword(s):

Salt Tolerance ◽

Protein Gene ◽

Ectopic Expression ◽

Lea Protein ◽

Thellungiella Salsuginea

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Chemical and Transcriptomic Analysis of Cuticle Lipids under Cold Stress in Thellungiella salsuginea

International Journal of Molecular Sciences ◽

10.3390/ijms20184519 ◽

2019 ◽

Vol 20 (18) ◽

pp. 4519 ◽

Cited By ~ 2

Author(s):

Junqing He ◽

Shuai Tang ◽

Di Yang ◽

Yue Chen ◽

Ludi Ling ◽

...

Keyword(s):

Cold Stress ◽

Transcriptomic Analysis ◽

Thellungiella Salsuginea ◽

Protective Layers ◽

Reverse Transcription Pcr ◽

Total Fatty Acids ◽

Wax Crystal ◽

The One ◽

The Relationship ◽

Cuticle Ultrastructure

Plant cuticle lipids form outer protective layers to resist environmental stresses; however, the relationship between cuticle properties and cold tolerance is unclear. Here, the extremophyte Thellungiella salsuginea was stressed under cold conditions (4 °C) and the cuticle of rosette leaves was examined in terms of epicuticular wax crystal morphology, chemical composition, and cuticle-associated gene expression. The results show that cold induced formation of distinct lamellas within the cuticle ultrastructure. Cold stress caused 14.58% and 12.04% increases in the amount of total waxes and cutin monomer per unit of leaf area, respectively, probably associated with the increase in total fatty acids. The transcriptomic analysis was performed on rosette leaves of Thellungiella exposed to cold for 24 h. We analyzed the expression of 72 genes putatively involved in cuticle lipid metabolism, some of which were validated by qRT-PCR (quantitative reverse transcription PCR) after both 24 h and one week of cold exposure. Most cuticle-associated genes exhibited higher expression levels under cold conditions, and some key genes increased more dramatically over the one week than after just 24 h, which could be associated with increased amounts of some cuticle components. These results demonstrate that the cuticle provides some aspects of cold adaptation in T. salsuginea.

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Acquisition of freezing tolerance in Arabidopsis and two contrasting ecotypes of the extremophile Eutrema salsugineum (Thellungiella salsuginea)

Journal of Plant Physiology ◽

10.1016/j.jplph.2015.03.011 ◽

2015 ◽

Vol 180 ◽

pp. 35-44 ◽

Cited By ~ 7

Author(s):

Nityananda Khanal ◽

Barbara A. Moffatt ◽

Gordon R. Gray

Keyword(s):

Freezing Tolerance ◽

Thellungiella Salsuginea ◽

Eutrema Salsugineum

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Distinct Roles for SOS1 in the Convergent Evolution of Salt Tolerance in Eutrema salsugineum and Schrenkiella parvula

Molecular Biology and Evolution ◽

10.1093/molbev/msu152 ◽

2014 ◽

Vol 31 (8) ◽

pp. 2094-2107 ◽

Cited By ~ 18

Author(s):

David E. Jarvis ◽

Choong-Hwan Ryu ◽

Mark A. Beilstein ◽

Karen S. Schumaker

Keyword(s):

Salt Tolerance ◽

Convergent Evolution ◽

Eutrema Salsugineum

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Growth irradiance affects ureide accumulation and tolerance to photoinhibition in Eutrema salsugineum (Thellungiella salsuginea)

Photosynthetica ◽

10.1007/s11099-015-0164-8 ◽

2016 ◽

Vol 54 (1) ◽

pp. 93-100 ◽

Cited By ~ 10

Author(s):

V. M. Malik ◽

J. M. Lobo ◽

C. Stewart ◽

S. Irani ◽

C. D. Todd ◽

...

Keyword(s):

Thellungiella Salsuginea ◽

Eutrema Salsugineum ◽

Growth Irradiance

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Exposure of two Eutrema salsugineum ( Thellungiella salsuginea ) accessions to water deficits reveals different coping strategies in response to drought

Physiologia Plantarum ◽

10.1111/ppl.12316 ◽

2015 ◽

Vol 155 (3) ◽

pp. 267-280 ◽

Cited By ~ 8

Author(s):

Mitchell J.R. MacLeod ◽

Jeff Dedrick ◽

Claire Ashton ◽

Wilson W.L. Sung ◽

Marc J. Champigny ◽

...

Keyword(s):

Coping Strategies ◽

Thellungiella Salsuginea ◽

Water Deficits ◽

Eutrema Salsugineum

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Transcriptome Profiling of the Salt Stress Response in the Leaves and Roots of Halophytic Eutrema salsugineum

Frontiers in Genetics ◽

10.3389/fgene.2021.770742 ◽

2021 ◽

Vol 12 ◽

Author(s):

Chuanshun Li ◽

Yuting Qi ◽

Chuanzhi Zhao ◽

Xingjun Wang ◽

Quan Zhang

Keyword(s):

Salt Stress ◽

Salt Tolerance ◽

Soluble Sugars ◽

Lignin Biosynthesis ◽

Sugar Metabolism ◽

Transcriptome Profiling ◽

Salt Stress Response ◽

Salt Shock ◽

Eutrema Salsugineum ◽

Leaves And Roots

Eutrema salsugineum can grow in natural harsh environments; however, the underlying mechanisms for salt tolerance of Eutrema need to be further understood. Herein, the transcriptome profiling of Eutrema leaves and roots exposed to 300 mM NaCl is investigated, and the result emphasized the role of genes involved in lignin biosynthesis, autophagy, peroxisome, and sugar metabolism upon salt stress. Furthermore, the expression of the lignin biosynthesis and autophagy-related genes, as well as 16 random selected genes, was validated by qRT-PCR. Notably, the transcript abundance of a large number of lignin biosynthesis genes such as CCoAOMT, C4H, CCR, CAD, POD, and C3′H in leaves was markedly elevated by salt shock. And the examined lignin content in leaves and roots demonstrated salt stress led to lignin accumulation, which indicated the enhanced lignin level could be an important mechanism for Eutrema responding to salt stress. Additionally, the differentially expressed genes (DEGs) assigned in the autophagy pathway including Vac8, Atg8, and Atg4, as well as DEGs enriched in the peroxisome pathway such as EsPEX7, EsCAT, and EsSOD2, were markedly induced in leaves and/or roots. In sugar metabolism pathways, the transcript levels of most DEGs associated with the synthesis of sucrose, trehalose, raffinose, and xylose were significantly enhanced. Furthermore, the expression of various stress-related transcription factor genes including WRKY, AP2/ERF-ERF, NAC, bZIP, MYB, C2H2, and HSF was strikingly improved. Collectively, the increased expression of biosynthesis genes of lignin and soluble sugars, as well as the genes in the autophagy and peroxisome pathways, suggested that Eutrema encountering salt shock possibly possess a higher capacity to adjust osmotically and facilitate water transport and scavenge reactive oxidative species and oxidative proteins to cope with the salt environment. Thus, this study provides a new insight for exploring the salt tolerance mechanism of halophytic Eutrema and discovering new gene targets for the genetic improvement of crops.

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The Salt Tolerance Related Protein (STRP) Mediates Cold Stress Responses and Abscisic Acid Signalling in Arabidopsis thaliana

Frontiers in Plant Science ◽

10.3389/fpls.2020.01251 ◽

2020 ◽

Vol 11 ◽

Author(s):

Anna Fiorillo ◽

Maurizio Mattei ◽

Patrizia Aducci ◽

Sabina Visconti ◽

Lorenzo Camoni

Keyword(s):

Arabidopsis Thaliana ◽

Abscisic Acid ◽

Salt Tolerance ◽

Cold Stress ◽

Stress Responses ◽

Related Protein

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Multiple paths lead to salt tolerance - pre-adaptation vs dynamic responses from two closely related extremophytes

10.1101/2021.10.23.465591 ◽

2021 ◽

Author(s):

Kieu-Nga Tran ◽

Guannan Wang ◽

Dong-Ha Oh ◽

John C. Larkin ◽

Aaron P Smith ◽

...

Keyword(s):

Salt Stress ◽

Salt Tolerance ◽

Stress Responses ◽

Crop Production ◽

Nutrient Balance ◽

Nutrient Content ◽

Dynamic Responses ◽

Metabolite Profiles ◽

Eutrema Salsugineum ◽

Multiple Paths

Salinity stress is an ongoing problem for global crop production. Schrenkiella parvula and Eutrema salsugineum are salt-tolerant extremophytes closely related to Arabidopsis thaliana. We investigated multi-omics salt stress responses of the two extremophytes in comparison to A. thaliana. Our results reveal that S. parvula limits Na accumulation while E. salsugineum shows high tissue tolerance to excess Na. Despite this difference, both extremophytes maintained their nutrient balance, while A. thaliana failed to sustain its nutrient content. The root metabolite profiles of the two extremophytes, distinct at control conditions, converged upon prolonged salt stress. This convergence was achieved by a dynamic response in S. parvula roots increasing its amino acids and sugars to the constitutively high basal levels observed in E. salsugineum. The metabolomic adjustments were strongly supported by the transcriptomic responses in the extremophytes. The predominant transcriptomic signals in all three species were associated with salt stress. However, root architecture modulation mediated by negative regulators of auxin and ABA signaling supported minimally affected root growth unique to each extremophyte during salt treatments. Overall, E. salsugineum exhibited more preadapted responses at the metabolome level while S. parvula showed predominant pre-adaptation at the transcriptome level to salt stress. Our work shows that while salt tolerance in these two species shares common features, they substantially differ in pathways leading to convergent adaptive traits.

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