Comparative Physiological and Transcriptome Analyses of Tolerant and Susceptible Cultivars Reveal the Molecular Mechanism of Cold Tolerance in Anthurium andraeanum
Abstract
:1. Introduction
2. Results
2.1. Cold Stress Triggers Morphological Differences between E and MH
2.2. Cold Stress Affects the Physiological Responses of E and MH
2.3. RNA Sequencing and De Novo Transcriptome Assembly
2.4. Functional Annotation of Unigenes
2.5. Differential Expression Analysis of Anthurium Genes
2.6. Functional Analysis of Common CSR DEGs in Anthurium
2.7. Co-Expression Network Analysis of DEGs
2.8. Plant Hormone Signal Transduction Is Involved in the Cold Stress Response in Anthurium
2.9. Trehalose-Related Genes Are Induced in Anthurium in Response to Cold Stress
2.10. Ribosomal Proteins Are Involved in Anthurium’s Response to Cold Stress
2.11. Validation of DEGs by qRT-PCR
3. Discussion
3.1. Morphological and Physiological Changes Differ between E and MH under Cold Stress
3.2. Plant Hormone Signal Transduction Pathways Are Important for Cold Response in Anthurium
3.3. Trehalose Metabolism in Anthurium Cold-Response
3.4. Ribosomal Proteins Play Important Roles in Cold Tolerance in Anthurium
3.5. HSP, Pectinesterase, and Plant Defense Proteins Are Commonly Involved in Anthurium Responses to Cold Stress
4. Materials and Methods
4.1. Plant Material and Stress Treatments
4.2. Determination of Enzyme Activity and MDA, Soluble Sugar, and Soluble Protein Contents
4.3. RNA Extraction and cDNA Library Construction
4.4. De Novo Transcriptome Assembly and Analysis
4.5. Identification of Key Modules Related to Plant Cold Stress by WGCNA
4.6. qRT-PCR Analysis
4.7. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Theocharis, A.; Clement, C.; Barka, E.A. Physiological and molecular changes in plants grown at low temperatures. Planta 2012, 235, 1091–1105. [Google Scholar] [CrossRef]
- Meng, S.; Xiang, H.; Yang, X.; Ye, Y.; Han, L.; Xu, T.; Liu, Y.; Wang, F.; Tan, C.; Qi, M.; et al. Effects of low temperature on pedicel abscission and auxin synthesis key genes of tomato. Int. J. Mol. Sci. 2023, 24, 9186. [Google Scholar] [CrossRef]
- Andaya, V.C.; Mackill, D.J. Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J. Exp. Bot. 2003, 54, 2579–2585. [Google Scholar] [CrossRef]
- Zuther, E.; Lee, Y.P.; Erban, A.; Kopka, J.; Hincha, D.K. Natural variation in freezing tolerance and cold acclimation response in Arabidopsis thaliana and related species. Adv. Exp. Med. Biol. 2018, 1081, 81–98. [Google Scholar]
- Valitova, J.; Renkova, A.; Mukhitova, F.; Dmitrieva, S.; Beckett, R.P.; Minibayeva, F.V. Membrane sterols and genes of sterol biosynthesis are involved in the response of Triticum aestivum seedlings to cold stress. Plant Physiol. Biochem. 2019, 142, 452–459. [Google Scholar] [CrossRef]
- Goswami, A.K.; Maurya, N.K.; Goswami, S.; Bardhan, K.; Singh, S.K.; Prakash, J.; Pradhan, S.; Kumar, A.; Chinnusamy, V.; Kumar, P.; et al. Physio-biochemical and molecular stress regulators and their crosstalk for low-temperature stress responses in fruit crops: A review. Front. Plant Sci. 2022, 13, 1022167. [Google Scholar] [CrossRef]
- Wang, S.; Zhao, H.; Zhao, L.; Gu, C.; Na, Y.; Xie, B.; Cheng, S.; Pan, G. Application of brassinolide alleviates cold stress at the booting stage of rice. J. Integ. Agric. 2020, 19, 975–987. [Google Scholar] [CrossRef]
- Wang, J.; Dong, S.; Jiang, Y.; He, H.; Liu, T.; Lv, M.; Shi, S. Influence of long-term cold storage on phenylpropanoid and soluble sugar metabolisms accompanied with peel browning of ‘Nanguo’ pears during subsequent shelf life. Sci. Hortic. 2020, 260, 108888. [Google Scholar] [CrossRef]
- Pinhero, R.G.; Rao, M.V.; Paliyath, G.; Murr, D.P.; Fletcher, R.A. Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiol. 1997, 114, 695–704. [Google Scholar] [CrossRef]
- Zhou, X.; Muhammad, I.; Lan, H.; Xia, C. Recent advances in the analysis of cold tolerance in maize. Front. Plant Sci. 2022, 13, 866034. [Google Scholar] [CrossRef] [PubMed]
- Fernandez, O.; Bethencourt, L.; Quero, A.; Sangwan, R.S.; Clement, C. Trehalose and plant stress responses: Friend or foe? Trends Plant Sci. 2010, 15, 409–417. [Google Scholar] [CrossRef] [PubMed]
- Lunn, J.E.; Delorge, I.; Figueroa, C.M.; Van Dijck, P.; Stitt, M. Trehalose metabolism in plants. Plant J. 2014, 79, 544–567. [Google Scholar] [CrossRef] [PubMed]
- Nawaz, M.; Hassan, M.U.; Chattha, M.U.; Mahmood, A.; Shah, A.N.; Hashem, M.; Alamri, S.; Batool, M.; Rasheed, A.; Thabit, M.A.; et al. Trehalose: A promising osmo-protectant against salinity stress-physiological and molecular mechanisms and future prospective. Mol. Biol. Rep. 2022, 49, 11255–11271. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Du, Y.; Yu, D. Trehalose phosphate synthase 5-dependent trehalose metabolism modulates basal defense responses in Arabidopsis thaliana. J. Integr. Plant Biol. 2019, 61, 509–527. [Google Scholar] [CrossRef] [PubMed]
- Li, H.W.; Zang, B.S.; Deng, X.W.; Wang, X.P. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 2011, 234, 1007–1018. [Google Scholar] [CrossRef] [PubMed]
- Van Houtte, H.; Vandesteene, L.; Lopez-Galvis, L.; Lemmens, L.; Kissel, E.; Carpentier, S.; Feil, R.; Avonce, N.; Beeckman, T.; Lunn, J.E.; et al. Overexpression of the trehalase gene AtTRE1 leads to increased drought stress tolerance in Arabidopsis and is involved in abscisic acid-induced stomatal closure. Plant Physiol. 2013, 161, 1158–1171. [Google Scholar] [CrossRef] [PubMed]
- Fichtner, F.; Lunn, J.E. The role of trehalose 6-phosphate (Tre6P) in plant metabolism and development. Annu. Rev. Plant Biol. 2021, 72, 737–760. [Google Scholar] [CrossRef] [PubMed]
- Baena-Gonzalez, E.; Lunn, J.E. SnRK1 and trehalose 6-phosphate-two ancient pathways converge to regulate plant metabolism and growth. Curr. Opin. Plant Biol. 2020, 55, 52–59. [Google Scholar] [CrossRef]
- Zhang, H.; Zhu, J.; Gong, Z.; Zhu, J.K. Abiotic stress responses in plants. Nat. Rev. Genet. 2022, 23, 104–119. [Google Scholar] [CrossRef]
- Dong, T.; Park, Y.; Hwang, I. Abscisic acid: Biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem. 2015, 58, 29–48. [Google Scholar]
- Li, X.Y.; Yang, Y.; Zhang, L.F.; Zuo, S.Y.; Li, L.J.; Jiao, J.; Li, J. Regulation on contents of endogenous hormones and Asr1 gene expression of maize seedling by exogenous ABA under low-temperature stress. ACTA Agron. Sin. 2017, 43, 141–148. [Google Scholar] [CrossRef]
- Tian, J.; Ma, Y.; Chen, Y.; Chen, X.; Wei, A. Plant hormone response to low-temperature stress in cold-tolerant and cold-sensitive varieties of Zanthoxylum bungeanum Maxim. Front. Plant Sci. 2022, 13, 847202. [Google Scholar] [CrossRef] [PubMed]
- Shibasaki, K.; Uemura, M.; Tsurumi, S.; Rahman, A. Auxin response in Arabidopsis under cold stress: Underlying molecular mechanisms. Plant Cell 2009, 21, 3823–3838. [Google Scholar] [CrossRef] [PubMed]
- Rahman, A. Auxin: A regulator of cold stress response. Physiol. Plant 2013, 147, 28–35. [Google Scholar] [CrossRef]
- Chaudhuri, A.; Halder, K.; Abdin, M.Z.; Majee, M.; Datta, A. Abiotic stress tolerance in plants: Brassinosteroids navigate competently. Int. J. Mol. Sci. 2022, 23, 14577. [Google Scholar] [CrossRef]
- Hu, Y.; Jiang, L.; Wang, F.; Yu, D. Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 2013, 25, 2907–2924. [Google Scholar] [CrossRef]
- Wang, Y.; Jiang, H.; Mao, Z.; Liu, W.; Jiang, S.; Xu, H.; Su, M.; Zhang, J.; Wang, N.; Zhang, Z.; et al. Ethylene increases the cold tolerance of apple via the MdERF1B-MdCIbHLH1 regulatory module. Plant J. 2021, 106, 379–393. [Google Scholar] [CrossRef]
- Fu, X.; Feng, Y.Q.; Zhang, X.W.; Zhang, Y.Y.; Bi, H.G.; Ai, X.Z. Salicylic acid is involved in rootstock-scion communication in improving the chilling tolerance of grafted cucumber. Front. Plant Sci. 2021, 12, 693344. [Google Scholar] [CrossRef]
- Kim, K.Y.; Park, S.W.; Chung, Y.S.; Chung, C.H.; Kim, J.I.; Lee, J.H. Molecular cloning of low-temperature-inducible ribosomal proteins from soybean. J. Exp. Bot. 2004, 55, 1153–1155. [Google Scholar] [CrossRef]
- Robles, P.; Quesada, V. Unveiling the functions of plastid ribosomal proteins in plant development and abiotic stress tolerance. Plant Physiol. Biochem. 2022, 189, 35–45. [Google Scholar] [CrossRef]
- Grennan, A.K.; Ort, D.R. Cool temperatures interfere with D1 synthesis in tomato by causing ribosomal pausing. Photosynth. Res. 2007, 94, 375–385. [Google Scholar] [CrossRef] [PubMed]
- Rogalski, M.; Schottler, M.A.; Thiele, W.; Schulze, W.X.; Bock, R. Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions. Plant Cell 2008, 20, 2221–2237. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Yuan, H.; Yang, Y.; Fish, T.; Lyi, S.M.; Thannhauser, T.W.; Zhang, L.; Li, L. Plastid ribosomal protein S5 is involved in photosynthesis, plant development, and cold stress tolerance in Arabidopsis. J. Exp. Bot. 2016, 67, 2731–2744. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.J.; Zheng, K.L.; Gong, X.D.; Xu, J.L.; Huang, J.R.; Lin, D.Z.; Dong, Y.J. The rice TCD11 encoding plastid ribosomal protein S6 is essential for chloroplast development at low temperature. Plant Sci. 2017, 259, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Liu, H.C.; Tian, D.Q.; Liu, J.X.; Ma, G.Y.; Zou, Q.C.; Zhu, Z.J. Cloning and functional analysis of a novel ascorbate peroxidase (APX) gene from Anthurium andraeanum. J. Zhejiang Univ. Sci. B 2013, 14, 1110–1120. [Google Scholar] [CrossRef] [PubMed]
- Tian, D.Q.; Pan, X.Y.; Yu, Y.M.; Wang, W.Y.; Zhang, F.; Ge, Y.Y.; Shen, X.L.; Shen, F.Q.; Liu, X.J. De novo characterization of the Anthurium transcriptome and analysis of its digital gene expression under cold stress. BMC Genom. 2013, 14, 827. [Google Scholar] [CrossRef] [PubMed]
- Jiang, L.; Tian, X.; Li, S.; Fu, Y.; Xu, J.; Wang, G. The AabHLH35 transcription factor identified from Anthurium andraeanum is involved in cold and drought tolerance. Plants 2019, 8, 216. [Google Scholar] [CrossRef] [PubMed]
- Jiang, L.; Fu, Y.; Sun, P.; Tian, X.; Wang, G. Identification of microRNA158 from Anthurium andraeanum and its function in cold stress tolerance. Plants 2022, 11, 3371. [Google Scholar] [CrossRef]
- Aghdam, M.S.; Naderi, R.; Jannatizadeh, A.; Babalar, M.; Sarcheshmeh, M.A.; Faradonbe, M.Z. Impact of exogenous GABA treatments on endogenous GABA metabolism in anthurium cut flowers in response to postharvest chilling temperature. Plant Physiol. Biochem. 2016, 106, 11–15. [Google Scholar] [CrossRef]
- Sun, X.; Yuan, Z.; Wang, B.; Zheng, L.; Tan, J.; Chen, F. Physiological and transcriptome changes induced by exogenous putrescine in anthurium under chilling stress. Bot. Stud. 2020, 61, 28. [Google Scholar] [CrossRef]
- Nadarajah, K.K. ROS homeostasis in abiotic stress tolerance in plants. Int. J. Mol. Sci. 2020, 21, 5208. [Google Scholar] [CrossRef] [PubMed]
- Gaweł, S.; Wardas, M.; Niedworok, E.; Wardas, P. Malondialdehyde (MDA) as a lipid peroxidation marker. Wiad. Lek. 2004, 57, 453–455. [Google Scholar] [PubMed]
- Jambunathan, N. Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. Methods Mol. Biol. 2010, 639, 292–298. [Google Scholar] [PubMed]
- Ristic, Z.; Ashworth, E. Changes in leaf ultrastructure and carbohydrates in Arabidopsis thaliana L.(Heyn) cv. Columbia during rapid cold acclimation. Protoplasma 1993, 172, 111–123. [Google Scholar] [CrossRef]
- Bliss, B.J.; Suzuki, J.Y. Genome size in Anthurium evaluated in the context of karyotypes and phenotypes. AoB Plants 2012, 2012, pls006. [Google Scholar] [CrossRef] [PubMed]
- Kang, S.H.; Lee, W.H.; Sim, J.S.; Thaku, N.; Chang, S.; Hong, J.P.; Oh, T.J. De novo transcriptome assembly of Senna occidentalis sheds light on the anthraquinone biosynthesis pathway. Front. Plant Sci. 2021, 12, 773553. [Google Scholar] [CrossRef] [PubMed]
- Langfelder, P.; Horvath, S. WGCNA: An R package for weighted correlation network analysis. BMC Bioinform. 2008, 9, 559. [Google Scholar] [CrossRef] [PubMed]
- Huang, Z.; Jin, S.H.; Guo, H.D.; Zhong, X.J.; He, J.; Li, X.; Jiang, M.Y.; Yu, X.F.; Long, H.; Ma, M.D.; et al. Genome-wide identification and characterization of TIFY family genes in Moso Bamboo (Phyllostachys edulis) and expression profiling analysis under dehydration and cold stresses. PeerJ 2016, 4, e2620. [Google Scholar] [CrossRef]
- Zhao, W.; Zheng, J.; Zhou, H.B. A thermotolerant and cold-active mannan endo-1,4-beta-mannosidase from Aspergillus niger CBS 513.88: Constitutive overexpression and high-density fermentation in Pichia pastoris. Bioresour. Technol. 2011, 102, 7538–7547. [Google Scholar] [CrossRef]
- Purohit, A.; Pawar, L.; Yadav, S.K. Structural and functional insights of a cold-adaptive beta-glucosidase with very high glucose tolerance from Microbacterium sp. CIAB417. Enzyme Microb. Technol. 2023, 169, 110284. [Google Scholar] [CrossRef]
- Rustgi, S.; Springer, A.; Kang, C.; von Wettstein, D.; Reinbothe, C.; Reinbothe, S.; Pollmann, S. ALLENE OXIDE SYNTHASE and HY DROPEROXIDE LYASE, two non-canonical cytochrome P450s in Arabidopsis thaliana and their different roles in plant defense. Int. J. Mol. Sci. 2019, 20, 3064. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Xu, Z.; Yin, W.; Xu, K.; Wang, S.; Shang, Q.; Sa, W.; Liang, J.; Wang, L. Genome-wide analysis of the Thaumatin-like gene family in Qingke (Hordeum vulgare L. var. nudum) uncovers candidates involved in plant defense against biotic and abiotic stresses. Front. Plant Sci. 2022, 13, 912296. [Google Scholar] [CrossRef] [PubMed]
- Verma, V.; Ravindran, P.; Kumar, P.P. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016, 16, 86. [Google Scholar] [CrossRef] [PubMed]
- Nishiyama, I. Male sterility caused by cooling treatment at the young microspore stage in rice plants. XII. Classification of tapetal hypertrophy on the basis of ultrastructure. Proc. Crop Sci. Soc. Jpn. 1976, 45, 254–262. [Google Scholar] [CrossRef]
- Medina, J.; Catala, R.; Salinas, J. The CBFs: Three arabidopsis transcription factors to cold acclimate. Plant Sci. 2011, 180, 3–11. [Google Scholar] [CrossRef] [PubMed]
- Ding, Y.; Yang, S. Surviving and thriving: How plants perceive and respond to temperature stress. Dev. Cell 2022, 57, 947–958. [Google Scholar] [CrossRef]
- Kumar, S.; Kaur, G.; Nayyar, H. Exogenous application of abscisic acid improves cold tolerance in chickpea (Cicer arietinum L.). J. Agron. Crop Sci. 2008, 194, 449–456. [Google Scholar] [CrossRef]
- Xue-Xuan, X.; Hong-Bo, S.; Yuan-Yuan, M.; Gang, X.; Jun-Na, S.; Dong-Gang, G.; Cheng-Jiang, R. Biotechnological implications from abscisic acid (ABA) roles in cold stress and leaf senescence as an important signal for improving plant sustainable survival under abiotic-stressed conditions. Crit. Rev. Biotechnol. 2010, 30, 222–230. [Google Scholar] [CrossRef]
- Eremina, M.; Rozhon, W.; Poppenberger, B. Hormonal control of cold stress responses in plants. Cell Mol. Life Sci. 2016, 73, 797–810. [Google Scholar] [CrossRef]
- Sun, M.; Shen, Y.; Chen, Y.; Wang, Y.; Cai, X.; Yang, J.; Jia, B.; Dong, W.; Chen, X.; Sun, X. Osa-miR1320 targets the ERF transcription factor OsERF096 to regulate cold tolerance via JA-mediated signaling. Plant Physiol. 2022, 189, 2500–2516. [Google Scholar] [CrossRef]
- Klay, I.; Gouia, S.; Liu, M.; Mila, I.; Khoudi, H.; Bernadac, A.; Bouzayen, M.; Pirrello, J. Ethylene Response Factors (ERF) are differentially regulated by different abiotic stress types in tomato plants. Plant Sci. 2018, 274, 137–145. [Google Scholar] [CrossRef] [PubMed]
- Huang, W.; Hu, B.; Liu, J.; Zhou, Y.; Liu, S. Identification and characterization of tonoplast sugar transporter (TST) gene family in cucumber. Hortic. Plant J. 2020, 6, 145–157. [Google Scholar] [CrossRef]
- Yang, T.; Huang, X.S. Deep sequencing-based characterization of transcriptome of Pyrus ussuriensis in response to cold stress. Gene 2018, 661, 109–118. [Google Scholar] [CrossRef] [PubMed]
- Mollavali, M.; Bornke, F. Characterization of trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase genes of tomato (Solanum lycopersicum L.) and analysis of their differential expression in response to temperature. Int. J. Mol. Sci. 2022, 23, 11436. [Google Scholar] [CrossRef] [PubMed]
- Frukh, A.; Siddiqi, T.O.; Khan, M.I.R.; Ahmad, A. Modulation in growth, biochemical attributes and proteome profile of rice cultivars under salt stress. Plant Physiol. Biochem. 2020, 146, 55–70. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Xu, Z.; Zhao, B.; Yang, Y.; Mi, J.; Zhao, Z.; Liu, J. Physiological and proteomic analysis responsive mechanisms for salt stress in oat. Front Plant Sci. 2022, 13, 891674. [Google Scholar] [CrossRef] [PubMed]
- Dumas, P.; Morin, M.D.; Boquel, S.; Moffat, C.E.; Morin, P.J. Expression status of heat shock proteins in response to cold, heat, or insecticide exposure in the Colorado potato beetle Leptinotarsa decemlineata. Cell Stress Chaperones 2019, 24, 539–547. [Google Scholar] [CrossRef]
- Chen, M.; Gan, L.; Zhang, J.; Shen, Y.; Qian, J.; Han, M.; Zhang, C.; Fan, J.; Sun, S.; Yan, X. A regulatory network of heat shock modules-photosynthesis-redox systems in response to cold stress across a latitudinal gradient in Bermudagrass. Front. Plant Sci. 2021, 12, 751901. [Google Scholar] [CrossRef]
- Eyles, S.J.; Gierasch, L.M. Nature’s molecular sponges: Small heat shock proteins grow into their chaperone roles. Proc. Natl. Acad. Sci. USA 2010, 107, 2727–2728. [Google Scholar] [CrossRef]
- Soto, A.; Allona, I.; Collada, C.; Guevara, M.A.; Casado, R.; Rodriguez-Cerezo, E.; Aragoncillo, C.; Gomez, L. Heterologous expression of a plant small heat-shock protein enhances Escherichia coli viability under heat and cold stress. Plant Physiol. 1999, 120, 521–528. [Google Scholar] [CrossRef]
- Cao, F.; Cheng, H.; Cheng, S.; Li, L.; Xu, F.; Yu, W.; Yuan, H. Expression of selected Ginkgo biloba heat shock protein genes after cold treatment could be induced by other abiotic stress. Int. J. Mol. Sci. 2012, 13, 5768–5788. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Hu, W.; Gao, Y.; Pan, H.; Zhang, Q. A cytosolic class II small heat shock protein, PfHSP17.2, confers resistance to heat, cold, and salt stresses in transgenic Arabidopsis. Genet. Mol. Biol. 2018, 41, 649–660. [Google Scholar] [CrossRef] [PubMed]
- Song, C.; Chung, W.S.; Lim, C.O. Overexpression of heat shock factor gene HsfA3 increases galactinol levels and oxidative stress tolerance in Arabidopsis. Mol. Cells 2016, 39, 477–483. [Google Scholar] [CrossRef] [PubMed]
- Goldberg, R.; Pierron, M.; Bordenave, M.; Breton, C.; Morvan, C.; du Penhoat, C.H. Control of mung bean pectinmethylesterase isoform activities. Influence of pH and carboxyl group distribution along the pectic chains. J. Biol. Chem. 2001, 276, 8841–8847. [Google Scholar] [CrossRef] [PubMed]
- Phan, T.D.; Bo, W.; West, G.; Lycett, G.W.; Tucker, G.A. Silencing of the major salt-dependent isoform of pectinesterase in tomato alters fruit softening. Plant Physiol. 2007, 144, 1960–1967. [Google Scholar] [CrossRef] [PubMed]
- Rautengarten, C.; Steinhauser, D.; Bussis, D.; Stintzi, A.; Schaller, A.; Kopka, J.; Altmann, T. Inferring hypotheses on functional relationships of genes: Analysis of the Arabidopsis thaliana subtilase gene family. PLoS Comput. Biol. 2005, 1, e40. [Google Scholar] [CrossRef] [PubMed]
- Figueiredo, A.; Monteiro, F.; Sebastiana, M. Subtilisin-like proteases in plant-pathogen recognition and immune priming: A perspective. Front. Plant Sci. 2014, 5, 739. [Google Scholar] [CrossRef]
- Grenzi, M.; Bonza, M.C.; Costa, A. Signaling by plant glutamate receptor-like channels: What else! Curr. Opin. Plant Biol. 2022, 68, 102253. [Google Scholar] [CrossRef]
- Yu, B.; Liu, N.; Tang, S.; Qin, T.; Huang, J. Roles of glutamate receptor-like channels (GLRs) in plant growth and response to environmental stimuli. Plants 2022, 11, 3450. [Google Scholar] [CrossRef]
- Li, H.; Jiang, X.; Lv, X.; Ahammed, G.J.; Guo, Z.; Qi, Z.; Yu, J.; Zhou, Y. Tomato GLR3.3 and GLR3.5 mediate cold acclimation-induced chilling tolerance by regulating apoplastic H2O2 production and redox homeostasis. Plant Cell Environ. 2019, 42, 3326–3339. [Google Scholar] [CrossRef]
- Pelagio-Flores, R.; Munoz-Parra, E.; Barrera-Ortiz, S.; Ortiz-Castro, R.; Saenz-Mata, J.; Ortega-Amaro, M.A.; Jimenez-Bremont, J.F.; Lopez-Bucio, J. The cysteine-rich receptor-like protein kinase CRK28 modulates Arabidopsis growth and development and influences abscisic acid responses. Planta 2019, 251, 2. [Google Scholar] [CrossRef] [PubMed]
- Mou, S.; Meng, Q.; Gao, F.; Zhang, T.; He, W.; Guan, D.; He, S. A cysteine-rich receptor-like protein kinase CaCKR5 modulates immune response against Ralstonia solanacearum infection in pepper. BMC Plant Biol 2021, 21, 382. [Google Scholar] [CrossRef] [PubMed]
- Cai, Z.Q.; Gao, Q. Comparative physiological and biochemical mechanisms of salt tolerance in five contrasting highland quinoa cultivars. BMC Plant Biol. 2020, 20, 70. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.; Zhou, Y.; Chen, Y.; Gu, J. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018, 34, i884–i890. [Google Scholar] [CrossRef] [PubMed]
- Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29, 644–652. [Google Scholar] [CrossRef]
- Patro, R.; Duggal, G.; Love, M.I.; Irizarry, R.A.; Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 2017, 14, 417–419. [Google Scholar] [CrossRef]
- Mortazavi, A.; Williams, B.A.; McCue, K.; Schaeffer, L.; Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 2008, 5, 621–628. [Google Scholar] [CrossRef]
- Robinson, M.D.; McCarthy, D.J.; Smyth, G.K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26, 139–140. [Google Scholar] [CrossRef]
- Buchfink, B.; Xie, C.; Huson, D.H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 2015, 12, 59–60. [Google Scholar] [CrossRef]
- Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N.S.; Wang, J.T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13, 2498–2504. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
Assembly Statistics | |
---|---|
Raw reads (average) | 47,943,471.56 |
Total number of clean reads | 840,806,398 |
Clean reads (average) | 46,711,466.56 |
Clean bases (G) | 117.67 |
Q20% (average) | 98.48 |
Q30% (average) | 95.09 |
GC% (average) | 51.42 |
Number of transcripts (˃200 bp) | 290,721 |
Number of unigenes | 132,108 |
Minimum length (bp) | 201 |
Maximum length (bp) | 16,127 |
Average length (bp) | 648 |
N50 length (bp) | 1207 |
GC content (%) | 44.84 |
Total assembled bases | 85,547,816 |
Four Common CSR-DEGs Upregulated in E but Downregulated in MH under 6 °C Stress | ||||
---|---|---|---|---|
Gene_ID | Name | log2FC (E_6 vs. E_CK) | log2FC (MH_6 vs. MH_CK) | Annotation |
TRINITY_DN43394_c2_g5 | - | 3.57 | −4.21 | - |
TRINITY_DN56057_c0_g5 | - | 2.68 | −3.36 | uncharacterized protein LOC110667824 [Hevea brasiliensis] |
TRINITY_DN42951_c1_g2 | - | 2.85 | −2.61 | - |
TRINITY_DN52943_c0_g2 | HSP17.4B | 3.55 | −2.42 | 17.4 kDa class III heat-shock protein [Phoenix dactylifera] |
Fifteen Common CSR-DEGs Upregulated in MH but Downregulated in E under 6 °C Stress | ||||
TRINITY_DN43741_c0_g2 | - | −3.28 | 4.19 | hypothetical protein L195_g017092, partial [Trifolium pratense] |
TRINITY_DN35319_c2_g1 | - | −2.04 | 3.91 | uncharacterized protein LOC18094378 isoform X3 [Populus trichocarpa] |
TRINITY_DN52379_c0_g2 | BURP3 | −3.76 | 9.79 | BURP domain-containing protein 3 [Phoenix dactylifera] |
TRINITY_DN39241_c0_g1 | SBT1.8 | −2.19 | 4.83 | hypothetical protein B296_00025367 [Ensete ventricosum] |
TRINITY_DN47085_c1_g1 | SBT1.6 | −2.05 | 4.74 | hypothetical protein B296_00025367 [Ensete ventricosum] |
TRINITY_DN42045_c2_g2 | SBT1.9 | −2.60 | 8.07 | subtilisin-like protease SBT1.9 [Phoenix dactylifera] |
TRINITY_DN35790_c0_g1 | COL16 | −5.34 | 3.72 | uncharacterized protein LOC111300501 [Durio zibethinus] |
TRINITY_DN37319_c0_g3 | GLR2.1 | −4.19 | 4.13 | PREDICTED: glutamate receptor 2.7-like [Elaeis guineensis] |
TRINITY_DN50258_c0_g4 | - | −2.25 | 4.23 | - |
TRINITY_DN55351_c1_g2 | CRK28 | −4.24 | 4.48 | hypothetical protein Ahy_B09g100047 isoform B [Arachis hypogaea] |
TRINITY_DN32295_c0_g1 | CRK6 | −3.10 | 4.38 | cysteine-rich receptor-like protein kinase 8 [Phoenix dactylifera] |
TRINITY_DN54550_c0_g1 | At3g47200 | −2.38 | 3.13 | PREDICTED: UPF0481 protein At3g47200-like [Elaeis guineensis] |
TRINITY_DN56023_c0_g2 | GLR2.2 | −2.30 | 6.76 | hypothetical protein AQUCO_03100069v1 [Aquilegia coerulea] |
TRINITY_DN56023_c0_g1 | GLR2.8 | −2.03 | 6.54 | Glutamate receptor 2.8 [Vitis vinifera] |
TRINITY_DN49565_c0_g3 | - | −3.55 | 3.72 | - |
Twenty-Seven Common CSR-DEGs Upregulated in E but Downregulated in MH under 4 °C Stress | ||||
---|---|---|---|---|
Gene_ID | Name | log2FC (E_4 vs. E_CK) | log2FC (MH_4 vs. MH_CK) | Annotation |
TRINITY_DN45412_c0_g4 | - | 4.33 | −4.71 | PREDICTED: uncharacterized protein LOC105048415 [Elaeis guineensis] |
TRINITY_DN56876_c2_g1 | - | 2.59 | −3.07 | - |
TRINITY_DN43394_c2_g5 | - | 4.86 | −3.71 | - |
TRINITY_DN52540_c1_g2 | PME1 | 3.65 | −4.19 | pectinesterase 3 [Jatropha curcas] |
TRINITY_DN56279_c2_g2 | - | 2.11 | −3.64 | - |
TRINITY_DN46551_c2_g2 | - | 2.65 | −3.66 | - |
TRINITY_DN35567_c1_g1 | HSFA2B | 3.09 | −9.03 | PREDICTED: heat shock factor protein HSF30-like [Elaeis guineensis] |
TRINITY_DN37079_c1_g3 | - | 6.35 | −3.61 | putative nucleotidyltransferase, Ribonuclease H [Rosa chinensis] |
TRINITY_DN36186_c0_g3 | TIP4-3 | 2.79 | −4.52 | PREDICTED: probable aquaporin TIP4-3 [Elaeis guineensis] |
TRINITY_DN36954_c1_g7 | - | 3.14 | −2.65 | - |
TRINITY_DN56438_c1_g1 | - | 5.30 | −2.24 | - |
TRINITY_DN51698_c0_g1 | - | 2.95 | −6.30 | - |
TRINITY_DN51173_c0_g1 | - | 2.56 | −3.04 | - |
TRINITY_DN33920_c1_g3 | FAAH | 2.87 | −3.55 | fatty acid amide hydrolase-like [Ananas comosus] |
TRINITY_DN54886_c1_g3 | - | 2.74 | −2.06 | - |
TRINITY_DN37706_c0_g1 | PME1 | 3.18 | −4.45 | pectinesterase 3 [Manihot esculenta] |
TRINITY_DN53485_c0_g2 | - | 4.42 | −3.28 | - |
TRINITY_DN54221_c0_g4 | - | 2.09 | −2.37 | - |
TRINITY_DN42775_c1_g1 | MPE3 | 2.80 | −3.45 | pectinesterase 1-like [Dendrobium catenatum] |
TRINITY_DN50024_c0_g1 | - | 2.61 | −2.82 | - |
TRINITY_DN42193_c0_g1 | - | 2.66 | −2.58 | PREDICTED: uncharacterized protein LOC105803676 [Gossypium raimondii] |
TRINITY_DN54864_c0_g4 | - | 2.61 | −2.85 | - |
TRINITY_DN42951_c1_g2 | - | 2.13 | −2.54 | - |
TRINITY_DN51579_c0_g3 | - | 2.18 | −2.27 | transcription factor MYBS3-like isoform X2 [Quercus suber] |
TRINITY_DN45042_c0_g3 | - | 2.06 | −3.21 | hypothetical protein AQUCO_05400137v1 [Aquilegia coerulea] |
TRINITY_DN52943_c0_g2 | HSP17.4B | 4.06 | −2.12 | 17.4 kDa class III heat-shock protein [Phoenix dactylifera] |
TRINITY_DN44614_c2_g1 | ELIP1 | 5.51 | −2.03 | chloroplastic early light-induced protein [Crocus sativus] |
Eight Common CSR-DEGs Downregulated in E but Upregulated in MH under 4 °C Stress | ||||
TRINITY_DN46057_c0_g4 | GPAT6 | −4.12 | 7.57 | Glycerol-3-phosphate 2-O-acyltransferase 6 [Ananas comosus] |
TRINITY_DN55055_c2_g2 | At1g61180 | −4.25 | 3.37 | probable disease resistance protein At5g63020 isoform X1 [Citrus sinensis] |
TRINITY_DN44362_c1_g2 | - | −2.86 | 3.86 | - |
TRINITY_DN49073_c0_g2 | - | −2.71 | 2.24 | - |
TRINITY_DN55351_c1_g2 | CRK28 | −3.46 | 3.54 | hypothetical protein Ahy_B09g100047 isoform B [Arachis hypogaea] |
TRINITY_DN39795_c1_g3 | - | −2.66 | 2.25 | PREDICTED: uncharacterized protein LOC109022142, partial [Juglans regia] |
TRINITY_DN45091_c1_g1 | CYP704C1 | −2.29 | 5.97 | PREDICTED: cytochrome P450 704C1-like [Elaeis guineensis] |
TRINITY_DN51899_c2_g3 | - | −4.76 | 7.31 | - |
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Dou, N.; Li, L.; Fang, Y.; Fan, S.; Wu, C. Comparative Physiological and Transcriptome Analyses of Tolerant and Susceptible Cultivars Reveal the Molecular Mechanism of Cold Tolerance in Anthurium andraeanum. Int. J. Mol. Sci. 2024, 25, 250. https://doi.org/10.3390/ijms25010250
Dou N, Li L, Fang Y, Fan S, Wu C. Comparative Physiological and Transcriptome Analyses of Tolerant and Susceptible Cultivars Reveal the Molecular Mechanism of Cold Tolerance in Anthurium andraeanum. International Journal of Molecular Sciences. 2024; 25(1):250. https://doi.org/10.3390/ijms25010250
Chicago/Turabian StyleDou, Na, Li Li, Yifu Fang, Shoujin Fan, and Chunxia Wu. 2024. "Comparative Physiological and Transcriptome Analyses of Tolerant and Susceptible Cultivars Reveal the Molecular Mechanism of Cold Tolerance in Anthurium andraeanum" International Journal of Molecular Sciences 25, no. 1: 250. https://doi.org/10.3390/ijms25010250