Transcriptome assembly, profiling and differential gene expression analysis of the halophyte Suaeda fruticosa provides insights into salt tolerance

Diray-Arce, Joann; Clement, Mark; Gul, Bilquees; Khan, M Ajmal; Nielsen, Brent L

doi:10.1186/s12864-015-1553-x

Table 3 Summary of selected differentially expressed genes in Suaeda fruticosa

From: Transcriptome assembly, profiling and differential gene expression analysis of the halophyte Suaeda fruticosa provides insights into salt tolerance

Differentially expressed Protein--‐coding genes ¹	Putative function or role in salt tolerance	Expression upon 300 mM salt treatment (upregulated or downregulated)	Plants with orthologous genes	References
General metabolism genes
Probable WRKY transcription factor 72	Sequence specific DNA binding transcription factor; Activators of ABA signaling Repressors of aleurone cells	Upregulated	Festuca rubra ssp litoralis	[22,25,69]
			Glycine soja
			Glycine max
			Oryza sativa
			Porteresia coarctata
WRKY transcription factor 6--like	Influence senescence and pathogen defense--‐associated PR1 promoter activity; mediates arsenate/phosphate transporter gene expression	Downregulated	Arabidopsis thaliana	[22,23,25,26]
			Festuca rubra ssp litoralis
			Glycine soja
			Glycine max
			Porteresia coarctata
WRKY DNA binding protein isoform 2	Transcription factors involved in various regulations; crucial to salinity tolerance	Downregulated	Festuca rubra ssp litoralis	[22-25,69]
			Glycine soja
			Glycine max
			Porteresia coarctata
Gibberellin 2--beta--‐dioxygenase 2 family (GA2OX2)	Gibberellin catabolic process; response to jasmonic acid and red light	Downregulated	Arabidopsis thaliana	[28,70,71]
40S ribosomal protein S4 (RPS4)	Disease resistance; SRP--‐dependent cotranslational protein	Upregulated	Arabidopsis thaliana	[72,73]
40S ribosomal protein S4 (RPS4)	Disease resistance; SRP--‐dependent cotranslational protein	Upregulated	Mesembryanthemum crystallinum	[72,73]
60S acidic ribosomal protein P2	Elongation step of protein synthesis	Upregulated	Zea mays	[30,74]
60S ribosomal protein L18–2--‐like	Plastidic and nuclear protein synthesis	Upregulated	Populus euphratica	[31,34]
60S ribosomal protein L18–2--‐like	Plastidic and nuclear protein synthesis	Upregulated	Suaeda maritima	[31,34]
Pre--mRNA processing protein 40C	Coactivator involved in the regulated transcription of nearly all RNA polymerase II--‐dependent genes	Downregulated	Arabidopsis thaliana	[30]
DNA--binding protein escarola--‐like	Late flowering and leaf development Leaf senescence	Upregulated	Arabidopsis thaliana	[30]
MADS--box transcription factor AGL24	Transcription activator that mediates floral transition in response to vernalizationl promotes inflorescence fate in apical meristem	Downregulated	Arabidopsis thaliana	[23,30]
MADS--box transcription factor AGL24		Downregulated	Porteresia coarctata	[23,30]
DNA binding protein with zinc finger isoform1	Binds DNA; structural regulation	Downregulated	Glycine max	[30,69,75]
			Malus zumi
			Arabidopsis thaliana
F--box protein AT1g78280--‐like transferase	Regulation of transcription; defense response by callose deposition	Downregulated	Arabidopsis thaliana	[30,34,76]
			Eutrema salsugineum
			Suaeda maritima
Glutathione--S--‐transferase tau 1	Glutathione metabolism; and production; promoted a higher level of salt tolerance	Upregulated	Arabidopsis thaliana	[2,31-33,35,36,69,77,78]
			Glycine max
			Glycine soja
			Nicotiana tabacum
			Populus euphratica
			Reaumuria trigyna
			Salicornia europaea
			Suaeda maritima
			Suaeda fruticosa
			Suaeda salsa
Germin--like protein	Salt--‐stress regulation marker	Upregulated	Arabidopsis thaliana	[37,38]
Germin--like protein	Salt--‐stress regulation marker	Upregulated	Hordeum vulgare	[37,38]
Flowering promoting factor 1--like protein 3	Regulates flowering time	Upregulated	Arabidopsis thaliana	[30]
Auxin--induced protein 5NG4--‐like	Transport of molecules functioning downstream of the auxin response; Root formation	Upregulated	Arabidopsis thaliana	[30]
Pathogenesis--related protein	Defense response; Response to water deprivation;	Upregulated	Arabidopsis thaliana	[30]
Chitinase	Enhance biotic and abiotic stress tolerance; reduce chitin in the cell wall contributing to salt sensitivity	Upregulated	Glycine max	[40,69]
			Glycine soja
			Nicotiana tabacum
Peroxisomal ascorbate peroxidase (APX)	Response to oxidative stress; Regeneration of NAD+; induced by high temperature	Upregulated	Nicotiana tabacum	[30,41]
Peroxisomal ascorbate peroxidase (APX)		Upregulated	Zea mays	[30,41]
Plant cadmium resistance 2--like	Reduces cadmium accumulation	Upregulated	Atriplex halimus	[42-44]
Chaperone protein DNAJ–16 like	Protein folding; protein partitioning into organelles; signal transduction; directly interacts with HSP70; induced by heat shock and prevents apoptosis	Downregulated	Arabidopsis thaliana	[34,45,46,79,80]
			Atriplex nummularia
			Suaeda maritima
			Spartina maritima
			Spartina alterniflora
Ethylene--responsive transcription factor rap2--‐7 like isoform	Transcriptional activator; binds to GCC box pathogenesis related promoter; Involved in the regulation of gene expression by stress factors; negatively regulates transition to flowering time	Downregulated	Arabidopsis thaliana	[30,34]
		Downregulated	Suaeda maritima	[30,34]
Senescence--associated protein	Induced by abscisic acid; regulated during natural and artificially induced leaf senescence	Downregulated	Arabidopsis thaliana	[72,81]
Senescence--associated protein		Downregulated	Mesembryanthemum crystallinum	[72,81]
Stem specific protein TSJT1--like	Stem--‐specific (active at lower levels in other organs)	Downregulated	Nicotiana tabacum	[30]
Protein F3H11–7	Positive regulation of transcription; leaf morphogenesis	Downregulated	Arabidopsis thaliana	[30]
Cell wall protein AWA1--like	Cell wall organization and biosynthesis	Downregulated	Theobroma cacao	[30]
Callose synthase 7	Callose synthesis at forming cell plate during cytokinesis; transitory component of the cell plate in dividing cells	Downregulated	Arabidopsis thaliana	[30]
Calcineurin B--like protein (CBL) 4--‐1	SOS like--‐gene; Acts as a calcium sensor involved in regulatory pathway for the control of Na + and K+ homeostasis and salt tolerance; Activates in synergy with CIPK24/SOS2 to activate Na+/H+ antiporter SOS1	Downregulated	Arabidopsis thaliana	[47,82,83]
Calcineurin B--like protein (CBL) 4--‐1		Downregulated	Eutrema salsugineum	[47,82,83]
Calmodulin binding isoform 1	Regulates transcriptional activity in response to calcium signals; activates the expression of the V--‐PPase proton pump in pollen	Downregulated	Arabidopsis thaliana	[47,48,69,84]
			Glycine max
			Glycine soja
			Leymus chinensis
Photosystem II protein z (PsbZ)	Controls photosystem II cores with the light-‐harvesting antenna	Upregulated	Arabidopsis thaliana	[30,72,75]
			Malus zumi
			Mesembryanthemum crystallinum
Photosystem D2 protein chloroplastic (psbD)	One of the two reaction center proteins of photosystem II; needed for assembly of a stable PSII complex	Upregulated	Arabidopsis thaliana	[30]
Photosystem II CP43 chlorophyll apoprotein (psbC)	Component of the core antenna complex of photosystem II; binds chlorophyll and helps catalyze the primary light--‐induced photochemical processes of photosystem II	Upregulated	Arabidopsis thaliana	[30]
Hypothetical Chloroplast RF19 (ycf1)	Unknown; may have a function which is probably not related to photosynthesis.	Upregulated	Arabidopsis thaliana	[30]
Zeaxanthin epoxidase, Chloroplastic--like isofom X2	Precursor to abscisic acid; involved in response to salt and heavy metal tolerance; required for resistance to osmotic and drought stresses, ABA--‐dependent stomatal closure, seed development and dormancy, modulation of defense gene expression; disease resistance	Upregulated	Arabidopsis thaliana	30,80]
			Spartina maritima
			Spartina alterniflora
Sufe--like chloroplastic like	Cysteine desulfurization in chloroplast and mitochondria; iron--‐sulfur cluster biosynthesis	Upregulated	Arabidopsis thaliana	[30]
High Light--induced chloroplastic protein	Possible role in chlorophyll and/or carotenoid binding	Downregulated	Arabidopsis thaliana	[30]
CRS2--associated factor chloroplastic like	Required for the splicing of group IIB introns in chloroplast; mRNA processing; intron specificity	Downregulated	Arabidopsis thaliana	[30]
CRS2--associated factor chloroplastic like		Downregulated	Zea mays	[30]
Thioredoxin--like protein z chloroplastic like	Redox regulation in the apoplast; cell division; cell differentiation; pollen germination; stress responses	Downregulated	Reaumuria trigyna	[32,80]
			Spartina alterniflora
			Spartina maritima
Triose phosphate chloroplastic like isoform X2	Exports photoassimilates from chloroplast; transports inorganic phosphate, 3--‐phosphoglycerate and triose phosphate	Downregulated	Arabidopsis thaliana	[30]
Probable chlorophyll b reductase chloroplastic--like	Chlorophyll B degradation	Downregulated	Arabidopsis thaliana	[30]
Phosphate chloroplastic like	Hypothetical protein	Downregulated	Arabidopsis thaliana	[30]
Ion transporters
Aquaporin tonoplast intrinsic protein 1	Water channel; facilitates the transport of water across cell membrane; osmoregulation; hydrogen peroxide transmembrane transport	Upregulated	Arabidopsis thaliana	[30,31,52,53,69,75,85]
			Glycine max
			Glycine soja
			Malus zumi
			Oryza sativa
			Populus euphratica
			Schrenkiella parvula
High affinity nitrate transporter 3.1 like	High--‐affinity nitrate transport; repressor of lateral root initiation; nitrate assimilation; response to wounding	Upregulated	Arabidopsis thaliana	[30]
High affinity nitrate transporter 3.1 like		Upregulated	Oryza sativa	[30]
Nitrate transporter 1.5	Transmembrane nitrate transporter; involved in xylem transport of nitrate from root to shoot; induced in response to nitrate	Upregulated	Arabidopsis thaliana	[30]
Aluminum--activated malate transporter 10	Malate transporter critical for aluminum tolerance; response to aluminum ion	Upregulated	Arabidopsis thaliana	[30]
Flavonol 4’--sulfotransferase, putative	Auxin transport; catalyze the sulfate conjugation	Upregulated	Flaveria chlorifolia	[30]
Bidirectional sugar transporter SWEET3	Mediates low affinity uptake and efflux of sugar across the plasma membrane	Upregulated	Arabidopsis thaliana	[30]
Glucosyltransferase	Catalyzes the glycosylation of flavonoids from UDP glucose	Upregulated	Arabidopsis thaliana	[30,31]
			Populus euphratica
			Populus pruinosa
Seed storage/lipid transfer protein	Bifunctional inhibitor/lipid transfer protein/seed storage 2S albumin superfamily	Upregulated	Arabidopsis thaliana	[30,31,86]
			Populus euphratica
			Thellungiella halophila
ATPase subunit 1 (chloroplast)	Maintainance of the pH of endomembrane compartments	Upregulated	Arabidopsis thaliana	[30]
			Leymus chinensis
			Thellungiella halophila
Sodium HKT1--like	Plant salt tolerance; response to salt and osmotic stress; involves in Na + recirculation; potassium ion transmembrane transporter	Downregulated	Arabidopsis thaliana	[30,32,33,53,86]
			Populus trichocarpa
			Reaumuria trigyna
			Salicornia europaea
			Schrenkiella parvula
			Thellungiella halophila
			Thellungiella salsuginea
Sodium pyruvate chloroplastic cotransporter	Pyruvate transport across chloroplast envelope	Downregulated	Arabidopsis thaliana	[30]
Magnesium transporter NIPA2	Magnesium ion transmembrane transport; can transport other divalent cations	Downregulated	Arabidopsis thaliana	[30]
Vacuolar Iron transporter family	Regulation of iron distribution; cellular response to ethylene stimulus; cellular response to nitric oxide; iron ion homeostasis; ion transport	Downregulated	Arabidopsis thaliana	[30]
Vacuolar proton ATPase A1--like	Essential component of the vacuolar proton pump (V--‐ATPase); cell expansion; ATP hydrolysis	Downregulated	Arabidopsis thaliana	[30,84]
Vacuolar proton ATPase A1--like		Downregulated	Leymus chinensis	[30,84]
ATPase ASNA1 homolog	Required for the post--‐translational delivery of tail anchored proteins to the endoplasmic reticulum; binds the transmembrane domain of tail--‐anchored proteins in the cytosol	Downregulated	Arabidopsis thaliana	[30]
Glutamyl--tRNA amidotransferase subunit chloroplastic mitochondrial--‐like	Allows the formation of correctly charged Gln--‐tRNA; ATP binding; glutaminyl--‐tRNAGln biosynthesis; mitochondrial translation	Downregulated	Arabidopsis thaliana	[30]
Tonoplast dicarboxylate transporter--like protein	Malate transmembrane transport; critical for pH homeostasis; indirectly involved in the uptake of malate and fumarate to the vacuole	Downregulated	Arabidopsis thaliana	[30]
Probable Galacturonosyltransferase 12-like	Involved in pectin assembly and/or distribution; cell wall organization	Downregulated	Arabidopsis thaliana	[30]
Regulatory molecules
Cysteine rich receptor like protein kinase	ATP binding; defense responses; disease resistance	Upregulated	Arabidopsis thaliana	[30]
Phosphatase 2C family protein	Stress responses; metal ion binding; protein dephosphorylation; Serine/threonine phosphatase activity	Downregulated	Arabidopsis thaliana	[30,31,58,69,80,87]
			Ceriops tagal
			Glycine max
			Glycine soja
			Populus trichocarpa
			Spartina maritima
			Spartina alterniflora
			Thellungiella salsuginea
Phosphatase 2C 76 isoform 1	Metal ion binding; Binds 2 magnesium or manganese ions	Downregulated	Arabidopsis thaliana	[30]
CDPK related kinase 1	Signal transduction pathways that involve calcium as second messenger; ATP binding; Ca2 + binding; protein autophosphorylation	Downregulated	Arabidopsis thaliana	[30,34,75,76]
			Eutrema salsugineum
			Malus zumi
			Suaeda maritima
PERK1 receptor protein kinase	Protein autophosphorylation; response to wounding; ATP binding	Downregulated	Arabidopsis thaliana	[30]
Casein kinase I--2--‐like protein	ATP binding; protein serine/threonine kinase activity	Downregulated	Arabidopsis thaliana	[30]
Serine--threonine protein kinase (histidine transporter) HT1	Control stomatal movement; shows a reduced response to ABA or light	Downregulated	Arabidopsis thaliana	[30,57]
		Downregulated	Oryza sativa	[30,57]
Phosphotidylinositol 4--kinase gamma 4	Phosphatidylinositol phosphorylation; Response to salt stress; Protein autophosphorylation	Downregulated	Arabidopsis thaliana	[30]
Serine threonine protein phosphatase pp1--like	Binds 2 manganese ions per subunit; protein dephosphorylation; serine/threonine phosphatase activity	Downregulated	Arabidopsis thaliana	[30]
Serine threonine--protein phosphatase PP2A catalytic subunit	Metal ion binding; serine/threonine phosphatase activity	Downregulated	Arabidopsis thaliana	[30]
Late embryogenesis abundant proteins
Dehydration--responsive RD22--‐like	Induced by salt stress; stress response	Upregulated	Malus zumi	[88]
			Populus euphratica
			Populus pruinosa
HSP20--like chaperones superfamily protein	Associated with stress and other abiotic factors	Downregulated	Glycine max	[89,90]
HSP20--like chaperones superfamily protein	Associated with stress and other abiotic factors	Downregulated	Oryza sativa	[89,90]

¹Identified and annotated using BLAST nr database using BLAST2GO.

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