Transcriptome Analysis of Chrysanthemum lavandulifolium Response to Salt Stress and Overexpression a K+ Transport ClAKT Gene-enhanced Salt Tolerance in Transgenic Arabidopsis

in Journal of the American Society for Horticultural Science

Plant growth and development are significantly affected by salt stress. Chrysanthemum lavandulifolium is a halophyte species and one of the ancestors of chrysanthemum (C. ×morifolium). Understanding how this species tolerates salt stress could provide vital insight for clarifying the salt response systems of higher plants, and chrysanthemum-breeding programs could be improved. In this study, salt tolerance was compared among C. lavandulifolium and three chrysanthemum cultivars by physiological experiments, among which C. lavandulifolium and Jinba displayed better tolerance to salt stress than the other two cultivars, whereas Xueshan was a salt-sensitive cultivar. Using the transcriptome database of C. lavandulifolium as a reference, we used digital gene expression technology to analyze the global gene expression changes in C. lavandulifolium seedlings treated with 200 mm NaCl for 12 hours compared with seedlings cultured in normal conditions. In total, 2254 differentially expressed genes (DEGs), including 1418 up-regulated and 836 down-regulated genes, were identified. These DEGs were significantly enriched in 35 gene ontology terms and 29 Kyoto Encyclopedia of Genes and Genomes pathways. Genes related to signal transduction, ion transport, proline biosynthesis, reactive oxygen species scavenging systems, and flavonoid biosynthesis pathways were relevant to the salt tolerance of C. lavandulifolium. Furthermore, comparative gene expression analysis was conducted using reverse transcription polymerase chain reaction to compare the transcriptional levels of significantly up-regulated DEGs in C. lavandulifolium and the salt-sensitive cultivar Xueshan, and species-specific differences were observed. The analysis of one of the DEGs, ClAKT, an important K+ transport gene, was found to enable transgenic Arabidopsis thaliana to absorb K+ and efflux Na+ under salt stress and to absorb K+ under drought stress. The present study investigated potential genes and pathways involved in salt tolerance in C. lavandulifolium and provided a hereditary resource for the confinement of genes and pathways responsible for salt tolerance in this species. This study provided a valuable source of reference genes for chrysanthemum cultivar transgenesis breeding.

Contributor Notes

This work was supported by the Fundamental Research Funds for the Central Universities (No. 2015ZCQ-YL-03) and National Natural Science Foundation of China (Grant no. 31501793).

These authors contributed equally.

Corresponding author. E-mail: silandai@sina.com.

Article Sections

Article Figures

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    Physiological response of Chrysanthemum lavandulifolium and C. ×morifolium ‘Xueshan’, ‘Xueshen’, and ‘Jinba’ leaves during salt treatment: (A) relative water content (RWC), (B) free proline content, (C) total flavonoids content, (D) chlorophyll content, (E) malondialdehyde (MDA) content, and (F) peroxidase (POD) activity.

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    (A) Distribution of unigene coverage in the control [CK (left)] and salt treatment samples [S1 (right)]. Different colors represent the percentage of different proportions of unigene coverage. The number of unigenes is indicated in parentheses. (B) Statistics of differentially expressed genes (DEGs). Different color column represent DEGs within diverse fold changes (Fold = Na200_RPKM/CK_RPKM); CK = seedlings were treated with clear water for 12 h; S1 = seedlings were treated with an equivalent amount of 200 mm NaCl for 12 h; RPKM = the reads per kilobase of transcript per million mapped reads.

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    Summary of differentially expressed genes (DEGs) using Blast2GO (Conesa et al., 2005). DEGs were classified into three main gene ontology [GO (Boyle et al., 2004)] annotations: cellular component (A), biological processes (B), and molecular functions (C). There are 36 GO terms for biological processes, 29 GO for molecular function, and 37 GO for cellular component.

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    Expression ratios of the 12 differentially expressed genes (DEGs) assessed by both digital gene expression (DGE) and quantitative real-time polymerase chain reaction (qRT-PCR) validation. PP2C = protein phosphatase 2C; MPK9 = MAP Kinase 9; SnRK2 = SNF1-related protein kinase 2; PT2 = phosphate transporter 2; ERF = ethylene-responsive transcription factor; bHLH1 = basic helix-loop-helix 1; MYB4 = myeloblastosis 4; bZIP = basic leucine zipper; C3HC4 = C3HC4 type zinc finger; HKT1 = high-affinity K+ transporter 1; F3′H1 = flavonoid 3′-hydroxylase.

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    (A) Comparative gene expression analysis by reverse transcription polymerase chain reaction was used to compare the transcriptional levels of 50 key salt-responsive genes in Chrysanthemum lavandulifolium and C. ×morifolium ‘Xueshan’ under salt treatment. (B) Heat map representation for expression of the genes. CBL = calcineurin B-like; CIPK = CBL-interacting protein kinase; MPK = MAP kinase; MAPKKK = mitogen-activated protein kinase kinase kinase; SnRK = SNF1-related protein kinase; PYL = abscisic acid receptor PYL; PP2C = protein phosphatase 2C; NCED = 9-cis-epoxycarotenoid dioxygenase; NAC = NAM, ATAF1/2, CUC2; VAP = vacuolar-type proton ATPase; NHX = Na+/H+ antiporter; AKT = Arabidopsis thaliana K+ transporter; HKT = high-affinity K+ transporter; ClC = chloride channel; RBOH = respiratory burst oxidase homologue; GST = glutathione-S-transferases; GRX = glutaredoxin; CAT = catalase; POD = peroxidase; P5CS = pyrroline-5-carboxylate synthetase; OAT = ornithine aminotransferase; PDH = phosphate dehydrogenase; PT2 = phosphate transporter 2; TPS = terpenoid synthase; TPP = trehalose-6-phosphatase; MYB = myeloblastosis; PAL = phenylalanine ammonia-lyase; CHS = chalcone synthase; CHI = chalcone isomerase; FNS = flavone synthase; FLS = flavonol synthase; F3′H = flavonoid 3′-hydroxylase; F3H = flavonoid 3-hydroxylase; DFR = dihydroflavonol 4-reductase; ANS = anthocyanidin synthase.

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    Bioinformation analysis of ClAKT2: (A) phylogenetic analysis and subfamilies classification; (B) transmembrane domains analysis of ClAKT (S represents the transmembrane domains); (C) transmembrane domains analysis of ClAKT (black rectangle represents the transmembrane domains and black points represent the anchor site); (D) comparison of the deduced amino acid sequence of ClAKT with its homologs (underline means the TxxTxGYGD motif of plants K+ channels). SKT1, CAA60016; LKT1, CAA65254; AKT1, NP_180233; TaAKT1, AAF36832; MKT1, AAF81249; SPIK, NP_180131; AKT6, NP_194976; MIRK, AAZ66349; SIRK, AAL09479; KST1, CAA56175; KAT1, NP_199436; KAT2, NP_193563; KCT2, AAX19659; NpKT1, BAA84085; SKT2, CAA70870; PTK2, CAC05489; AKT2, NP_567651; SPICK2, AAD39492; VfK1, CAA71598; SPICK1, AAD16278; AtKC1, NP_194991; KDC1, CAB62555.

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    Phenotype of wild-type (WT) and ClAKT2-expressing Arabidopsis thaliana. (A) seedlings of WT and A2 and A10 were germinated on a 1/2 Murashige and Skoog (MS) agar plate supplemented with different abiotic stresses. The relative root (B) length and (C) numbers of lateral root of WT and 35S-ClAKT seedlings treated by different abiotic stresses in comparison with control seedlings. A2 = 35S-ClAKT transgenic A. thaliana line 2; A10 = 35S-ClAKT transgenic A. thaliana line 10. CK = 1/2 MS, Na: 1/2 MS+100 Na, +Na-K: 1/2 MS-K+50 Na, −K: 1/2 MS-K, 2Na: 1/2 MS+200 Na.

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    Effect of ClAKT2 overexpression on growth of Arabidopsis thaliana (A) and Na+, K+ content in different plant organs (B) under salt treatment. Effect of ClAKT overexpression on growth of A. thaliana (C) and Na+, K+ content in different plant organs (D) under drought treatment. The numbers on the x-axis of A and C are these plants survival numbers. WT = wild type; A2 = 35S-ClAKT transgenic A. thaliana line 2; A10 = 35S-ClAKT transgenic A. thaliana line 10.

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    A proposed model revealing the potential mechanism of salt stress response in Chrysanthemum lavandulifolium. PYL = pyrabactin resistance 1-like; RCAR-PP2C = RCAR-protein phosphatase 2C; cADPR = cyclic adenosine diphosphate (ADP)-ribose; SnRK2 = SNF1-related protein kinase 2; RBOH = respiratory burst oxidase homologue; CaM = calmodulin; CDPK = calcium-dependent protein kinase; NAC = NAM, ATAF1/2, CUC2; TF = transcription factors; POD = peroxidase; CAT = catalase; CBL = calcineurin B-like protein; CPK = calcium-dependent protein kinase; SOS1 = Salt Overly Sensitively 1; AKT1 = Arabidopsis thaliana K+ transporter; CNGC = cyclic-nucleotide gated channel; V-ATPase = vacuolar- ATPase; MAP = mitogen-activated protein; MAPK = mitogen-activated protein kinase; MAPKK = mitogen-activated protein kinase kinase; ROS = responsive oxygen species.

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