Identification of cysteine-rich receptor-like kinase gene family in potato: revealed StCRLK9 in response to heat, salt and drought stresses
Roshan Zameer
A * , Khairiah Mubarak Alwutayd B , Dikhnah Alshehri C , Muhammad Salman Mubarik D , Cheng Li A , Chengde Yu A * and Zhifang Li A *
A
B
C
D
Handling Editor: Sajid Fiaz
Abstract
The investigation into cysteine-rich receptor-like kinases (CRLKs) holds pivotal significance as these conserved, upstream signalling molecules intricately regulate fundamental biological processes such as plant growth, development and stress adaptation. This study undertakes a comprehensive characterisation of CRLKs in Solanum tuberosum (potato), a staple food crop of immense economic importance. Employing comparative genomics and evolutionary analyses, we identified 10 distinct CRLK genes in potato. Further categorisation into three major groups based on sequence similarity was performed. Each CRLK member in potato was systematically named according to its chromosomal position. Multiple sequence alignment and phylogenetic analyses unveiled conserved gene structures and motifs within the same groups. The genomic distribution of CRLKs was observed across Chromosomes 2–5, 8 and 12. Gene duplication analysis highlighted a noteworthy trend, with most gene pairs exhibiting a Ka/Ks ratio greater than one, indicating positive selection of StCRLKs in potato. Salt and drought stresses significantly impacted peroxidase and catalase activities in potato seedlings. The presence of diverse cis-regulatory elements, including hormone-responsive elements, underscored their involvement in myriad biotic and abiotic stress responses. Interestingly, interactions between the phytohormone auxin and CRLK proteins unveiled a potential auxin-mediated regulatory mechanism. A holistic approach combining transcriptomics and quantitative PCR validation identified StCRLK9 as a potential candidate involved in plant response to heat, salt and drought stresses. This study lays a robust foundation for future research on the functional roles of the CRLK gene family in potatoes, offering valuable insights into their diverse regulatory mechanisms and potential applications in stress management.
Keywords: 3D structure, abiotic stresses, auxin, CRLKs, docking, expression, Solanum tuberosum.
References
Acharya BR, Raina S, Maqbool SB, Jagadeeswaran G, Mosher SL, Appel HM, Schultz JC, Klessig DF, Raina R (2007) Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae. The Plant Journal 50, 488-499.
| Crossref | Google Scholar | PubMed |
Azeem F, Ijaz U, Ali MA, Hussain S, Zubair M, Manzoor H, Abid M, Zameer R, Kim D-S, Golokhvast KS, Chung G, Sun S, Nawaz MA (2021) Genome-wide identification and expression profiling of potassium transport-related genes in Vigna radiata under abiotic stresses. Plants 11(1), 2.
| Crossref | Google Scholar |
Bae S-H, Han HW, Moon J (2015) Functional analysis of the molecular interactions of TATA box-containing genes and essential genes. PLoS ONE 10, e0120848.
| Crossref | Google Scholar | PubMed |
Baek D, Kim MC, Kumar D, Park B, Cheong MS, Choi W, Park HC, Chun HJ, Park HJ, Lee SY, Bressan RA, Kim J-Y, Yun D-J (2019) AtPR5K2, a PR5-Like receptor kinase, modulates plant responses to drought stress by phosphorylating protein phosphatase 2Cs. Frontiers in Plant Science 10, 1146.
| Crossref | Google Scholar |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
| Crossref | Google Scholar | PubMed |
Burdiak P, Rusaczonek A, Witoń D, Głów D, Karpiński S (2015) Cysteine-rich receptor-like kinase CRK5 as a regulator of growth, development, and ultraviolet radiation responses in Arabidopsis thaliana. Journal of Experimental Botany 66, 3325-3337.
| Crossref | Google Scholar | PubMed |
Campos Mantello C, Boatwright L, da Silva CC, Scaloppi EJ, de Souza Goncalves P, Barbazuk WB, Pereira de Souza A (2019) Deep expression analysis reveals distinct cold-response strategies in rubber tree (Hevea brasiliensis). BMC Genomics 20, 455.
| Crossref | Google Scholar |
Caumon H, Vernoux T (2023) A matter of time: auxin signaling dynamics and the regulation of auxin responses during plant development. Journal of Experimental Botany 74, 3887-3902.
| Crossref | Google Scholar |
Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Methods in Enzymology 2, 764-775.
| Crossref | Google Scholar |
Charfeddine M, Chiab N, Charfeddine S, Ferjani A, Gargouri-Bouzid R (2023) Heat, drought, and combined stress effect on transgenic potato plants overexpressing the StERF94 transcription factor. Journal of Plant Research 136, 549-562.
| Crossref | Google Scholar | PubMed |
Chen Z (2001) A superfamily of proteins with novel cysteine-rich repeats. Plant Physiology 126, 473-476.
| Crossref | Google Scholar | PubMed |
Chen K, Du L, Chen Z (2003) Sensitization of defense responses and activation of programmed cell death by a pathogen-induced receptor-like protein kinase in Arabidopsis. Plant Molecular Biology 53, 61-74.
| Crossref | Google Scholar | PubMed |
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13, 1194-1202.
| Crossref | Google Scholar |
Chern M, Xu Q, Bart RS, Bai W, Ruan D, Sze-To WH, Canlas PE, Jain R, Chen X, Ronald PC (2016) A genetic screen identifies a requirement for cysteine-rich–receptor-like kinases in rice NH1 (OsNPR1)-mediated immunity. PLoS Genetics 12, e1006049.
| Crossref | Google Scholar | PubMed |
Cui Y, Lu X, Gou X (2022) Receptor-like protein kinases in plant reproduction: current understanding and future perspectives. Plant Communications 3, 100273.
| Crossref | Google Scholar |
Czernic P, Visser B, Sun W, Savouré A, Deslandes L, Marco Y, Van Montagu M, Verbruggen N (1999) Characterization of an Arabidopsis thaliana receptor-like protein kinase gene activated by oxidative stress and pathogen attack. The Plant Journal 18, 321-327.
| Crossref | Google Scholar | PubMed |
Deblonde PMK, Ledent J-F (2001) Effects of moderate drought conditions on green leaf number, stem height, leaf length and tuber yield of potato cultivars. European Journal of Agronomy 14, 31-41.
| Crossref | Google Scholar |
Feng H-L, Ma N-N, Meng X, Zhang S, Wang J-R, Chai S, Meng Q-W (2013) A novel tomato MYC-type ICE1-like transcription factor, SlICE1a, confers cold, osmotic and salt tolerance in transgenic tobacco. Plant Physiology and Biochemistry 73, 309-320.
| Crossref | Google Scholar | PubMed |
Gu J, Sun J, Liu N, Sun X, Liu C, Wu L, Liu G, Zeng F, Hou C, Han S, Zhen W, Wang D (2020) A novel cysteine-rich receptor-like kinase gene, TaCRK2, contributes to leaf rust resistance in wheat. Molecular Plant Pathology 21, 732-746.
| Crossref | Google Scholar | PubMed |
Gómez-Porras JL, Riaño-Pachón DM, Dreyer I, Mayer JE, Mueller-Roeber B (2007) Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC Genomics 8, 260.
| Crossref | Google Scholar |
Han X, Yang R, Zhang L, Wei Q, Zhang Y, Wang Y, Shi Y (2023) A review of potato salt tolerance. International Journal of Molecular Sciences 24, 10726.
| Crossref | Google Scholar |
Hill D, Nelson D, Hammond J, Bell L (2021) Morphophysiology of potato (Solanum tuberosum) in response to drought stress: paving the way forward. Frontiers in Plant Science 11, 597554.
| Crossref | Google Scholar |
Huang Y, Gao B, Huang W, Wang L, Fang X, Xu S, Cui S (2021) Producing more potatoes with lower inputs and greenhouse gases emissions by regionalized cooperation in China. Journal of Cleaner Production 299, 126883.
| Crossref | Google Scholar |
Hunter K, Kimura S, Rokka A, Tran HC, Toyota M, Kukkonen JP, Wrzaczek M (2019) CRK2 enhances salt tolerance by regulating callose deposition in connection with PLD α 1. Plant Physiology 180, 2004-2021.
| Crossref | Google Scholar | PubMed |
Idänheimo N, Gauthier A, Salojärvi J, Siligato R, Brosché M, Kollist H, Mähönen AP, Kangasjärvi J, Wrzaczek M (2014) The Arabidopsis thaliana cysteine-rich receptor-like kinases CRK6 and CRK7 protect against apoplastic oxidative stress. Biochemical and Biophysical Research Communications 445, 457-462.
| Crossref | Google Scholar | PubMed |
Ijaz U, Pervaiz T, Ahmed T, Seemab R, Shahid M, Noman M, Nadeem M, Azeem F (2023) AJAB. Asian Journal of Agriculture & Biology 4(4), 2023110.
| Google Scholar |
Jing Q, Hou H, Meng X, Chen A, Wang L, Zhu H, Zheng S, Lv Z, Zhu X (2022) Transcriptome analysis reveals the proline metabolic pathway and its potential regulation TF-hub genes in salt-stressed potato. Frontiers in Plant Science 13, 1030138.
| Crossref | Google Scholar | PubMed |
Jinjun Z, Peina J, Fang Z, Chongke Z, Bo B, Yaping L, Haifeng W, Fan C, Xianzhi X (2020) OsSRK1, an Atypical S-receptor-like kinase positively regulates leaf width and salt tolerance in rice. Rice Science 27, 133-142.
| Crossref | Google Scholar |
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, Bridgland A, Meyer C, Kohl SAA, Ballard AJ, Cowie A, Romera-Paredes B, Nikolov S, Jain R, Adler J, Back T, Petersen S, Reiman D, Clancy E, Zielinski M, Steinegger M, Pacholska M, Berghammer T, Bodenstein S, Silver D, Vinyals O, Senior AW, Kavukcuoglu K (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596, 583-589.
| Crossref | Google Scholar | PubMed |
Kolachevskaya OO, Sergeeva LI, Floková K, Getman IA, Lomin SN, Alekseeva V V, Rukavtsova EB, Buryanov YI, Romanov GA (2017) Auxin synthesis gene tms1 driven by tuber-specific promoter alters hormonal status of transgenic potato plants and their responses to exogenous phytohormones. Plant Cell Reports 36, 419-435.
| Crossref | Google Scholar | PubMed |
Kolachevskaya OO, Lomin SN, Arkhipov DV, Romanov GA (2019) Auxins in potato: molecular aspects and emerging roles in tuber formation and stress resistance. Plant Cell Reports 38, 681-698.
| Crossref | Google Scholar | PubMed |
Kono Y (1978) Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Archives of Biochemistry and Biophysics 186, 189-195.
| Crossref | Google Scholar | PubMed |
Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. The Plant Cell 22, 3574-3588.
| Crossref | Google Scholar | PubMed |
Kumar S, Asrey R, Mandal G (2007) Effect of differential irrigation regimes on potato (Solanum tuberosum) yield and post-harvest attributes. Indian Journal of Agricultural Sciences 77(6), 336-338.
| Google Scholar |
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870-1874.
| Crossref | Google Scholar | PubMed |
Lager I, Andréasson O, Dunbar TL, Andreasson E, Escobar MA, Rasmusson AG (2010) Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses. Plant, Cell & Environment 33, 1513-1528.
| Crossref | Google Scholar | PubMed |
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357-359.
| Crossref | Google Scholar |
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30, 325-327.
| Crossref | Google Scholar | PubMed |
Li T-G, Zhang D-D, Zhou L, Kong Z-Q, Hussaini AS, Wang D, Li J-J, Short DPG, Dhar N, Klosterman SJ, Wang BL, Yin CM, Subbarao KV, Chen JY, Dai XF (2018) Genome-wide identification and functional analyses of the CRK gene family in cotton reveals GbCRK18 confers verticillium wilt resistance in Gossypium barbadense. Frontiers in Plant Science 9, 1266.
| Crossref | Google Scholar | PubMed |
Li J, Han G, Sun C, Sui N (2019) Research advances of MYB transcription factors in plant stress resistance and breeding. Plant Signaling & Behavior 14, 1613131.
| Crossref | Google Scholar | PubMed |
Li X, Shen F, Xu X, Zheng Q, Wang Y, Wu T, Li W, Qiu C, Xu X, Han Z, Zhang X (2021) An HD-ZIP transcription factor, MxHB13, integrates auxin-regulated and juvenility-determined control of adventitious rooting in Malus xiaojinensis. The Plant Journal 107, 1663-1680.
| Crossref | Google Scholar | PubMed |
Liu Y, Zhang C, Chen J, Guo L, Li X, Li W, Yu Z, Deng J, Zhang P, Zhang K, Zhang L (2013) Arabidopsis heat shock factor HsfA1a directly senses heat stress, pH changes, and hydrogen peroxide via the engagement of redox state. Plant Physiology and Biochemistry 64, 92-98.
| Crossref | Google Scholar | PubMed |
Liu Y, Feng Z, Zhu W, Liu J, Zhang Y (2021) Genome-wide identification and characterization of cysteine-rich receptor-like protein kinase genes in tomato and their expression profile in response to heat stress. Diversity 13, 258.
| Crossref | Google Scholar |
Liu J, Li W, Wu G, Ali K (2024) An update on evolutionary, structural, and functional studies of receptor-like kinases in plants. Frontiers in Plant Science 15, 1305599.
| Crossref | Google Scholar |
Lu K, Liang S, Wu Z, Bi C, Yu Y-T, Wang X-F, Zhang D-P (2016) Overexpression of an Arabidopsis cysteine-rich receptor-like protein kinase, CRK5, enhances abscisic acid sensitivity and confers drought tolerance. Journal of Experimental Botany 67, 5009-5027.
| Crossref | Google Scholar | PubMed |
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15-19.
| Crossref | Google Scholar | PubMed |
Miyakawa T, Miyazono K, Sawano Y, Hatano K, Tanokura M (2009) Crystal structure of ginkbilobin-2 with homology to the extracellular domain of plant cysteine-rich receptor-like kinases. Proteins: Structure, Function, and Bioinformatics 77, 247-251.
| Crossref | Google Scholar |
Nanda S, Rout P, Ullah I, Nag SR, Reddy VV, Kumar G, Kumar R, He S, Wu H (2023) Genome-wide identification and molecular characterization of CRK gene family in cucumber (Cucumis sativus L.) under cold stress and sclerotium rolfsii infection. BMC Genomics 24, 219.
| Crossref | Google Scholar | PubMed |
Nasir MW, Toth Z (2022) Effect of drought stress on potato production: a review. Agronomy 12, 635.
| Crossref | Google Scholar |
Ou Y, Kui H, Li J (2021) Receptor-like kinases in root development: current progress and future directions. Molecular Plant 14, 166-185.
| Crossref | Google Scholar | PubMed |
Pelagio-Flores R, Muñoz-Parra E, Barrera-Ortiz S, Ortiz-Castro R, Saenz-Mata J, Ortega-Amaro MA, Jiménez-Bremont JF, López-Bucio J (2020) The cysteine-rich receptor-like protein kinase CRK28 modulates Arabidopsis growth and development and influences abscisic acid responses. Planta 251, 1-12.
| Crossref | Google Scholar |
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25, 1605-1612.
| Crossref | Google Scholar | PubMed |
Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5, 308-316.
| Crossref | Google Scholar | PubMed |
Pérez-de-Castro AM, Vilanova S, Cañizares J, Pascual L, Blanca JM, Diez MJ, Prohens J, Picó B (2012) Application of genomic tools in plant breeding. Current Genomics 13, 179-195.
| Crossref | Google Scholar |
Rahnama H, Ebrahimzadeh H (2005) The effect of NaCl on antioxidant enzyme activities in potato seedlings. Biologia Plantarum 49, 93-97.
| Crossref | Google Scholar |
Rout SS, Rout P, Uzair M, Kumar G, Nanda S (2023) Genome-wide identification and expression analysis of CRK gene family in chili pepper (Capsicum annuum L.) in response to Colletotrichum truncatum infection. The Journal of Horticultural Science and Biotechnology 98, 194-206.
| Crossref | Google Scholar |
Rozas J, Ferrer-mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 3299-3302.
| Crossref | Google Scholar |
Sakamoto T, Morinaka Y, Inukai Y, Kitano H, Fujioka S (2013) Auxin signal transcription factor regulates expression of the brassinosteroid receptor gene in rice. The Plant Journal 73, 676-688.
| Crossref | Google Scholar | PubMed |
Sarwar R, Li L, Yu J, Zhang Y, Geng R, Meng Q, Zhu K, Tan X-L (2023) Functional characterization of the cystine-rich-receptor-like kinases (CRKs) and their expression response to Sclerotinia sclerotiorum and abiotic stresses in Brassica napus. International Journal of Molecular Sciences 24, 511.
| Crossref | Google Scholar | PubMed |
Shabala S, Wu H, Bose J (2015) Salt stress sensing and early signalling events in plant roots: current knowledge and hypothesis. Plant Science 241, 109-119.
| Crossref | Google Scholar | PubMed |
Shafique A, Batool R, Rizwan M, Zameer R, Arshad H, Xu H, Alwutayd K, AbdElgawad H, Azeem F (2023) Integrative omics analysis of Rosa chinensis reveals insights into its transcriptome and in silico characterization of potassium transport genes. Plant Stress 10, 100202.
| Crossref | Google Scholar |
Shani E, Salehin M, Zhang Y, Sanchez SE, Doherty C, Wang R, Mangado CC, Song L, Tal I, Pisanty O, Ecker JR, Kay SA, Pruneda-Paz J, Estelle M (2017) Plant stress tolerance requires auxin-sensitive Aux/IAA transcriptional repressors. Current Biology 27, 437-444.
| Crossref | Google Scholar | PubMed |
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13, 2498-2504.
| Crossref | Google Scholar | PubMed |
Shapiguzov A, Vainonen JP, Wrzaczek M, Kangasjärvi J (2012) ROS-talk–how the apoplast, the chloroplast, and the nucleus get the message through. Frontiers in Plant Science 3, 292.
| Crossref | Google Scholar |
Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. The Plant Cell 19, 2440-2453.
| Crossref | Google Scholar | PubMed |
Shiu S-H, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiology 132, 530-543.
| Crossref | Google Scholar | PubMed |
Shiu S-H, Karlowski WM, Pan R, Tzeng Y-H, Mayer KFX, Li W-H (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. The Plant Cell 16, 1220-1234.
| Crossref | Google Scholar | PubMed |
Shu W, Zhou H, Jiang C, Zhao S, Wang L, Li Q, Yang Z, Groover A, Lu M-Z (2019) The auxin receptor TIR 1 homolog (Pag FBL 1) regulates adventitious rooting through interactions with Aux/IAA 28 in Populus. Plant Biotechnology Journal 17, 338-349.
| Crossref | Google Scholar | PubMed |
Shumayla , Tyagi S, Sharma A, Singh K, Upadhyay SK (2019) Genomic dissection and transcriptional profiling of cysteine-rich receptor-like kinases in five cereals and functional characterization of TaCRK68-A. International Journal of Biological Macromolecules 134, 316-329.
| Crossref | Google Scholar |
Tanaka H, Osakabe Y, Katsura S, Mizuno S, Maruyama K, Kusakabe K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) Abiotic stress-inducible receptor-like kinases negatively control ABA signaling in Arabidopsis. The Plant Journal 70, 599-613.
| Crossref | Google Scholar | PubMed |
Tang R, Zhu W, Song X, Lin X, Cai J, Wang M, Yang Q (2016) Genome-wide identification and function analyses of heat shock transcription factors in potato. Frontiers in Plant Science 7, 490.
| Google Scholar | PubMed |
Tang R, Niu S, Zhang G, Chen G, Haroon M, Yang Q, Rajora OP, Li X-Q (2018) Physiological and growth responses of potato cultivars to heat stress. Botany 96, 897-912.
| Crossref | Google Scholar |
Tao J, Wu F, Wen H, Liu X, Luo W, Gao L, Jiang Z, Mo B, Chen X, Kong W, Yu Y (2023) RCD1 promotes salt stress tolerance in Arabidopsis by repressing ANAC017 activity. International Journal of Molecular Sciences 24, 9793.
| Crossref | Google Scholar | PubMed |
Theine J, Holtgräwe D, Herzog K, Schwander F, Kicherer A, Hausmann L, Viehöver P, Töpfer R, Weisshaar B (2021) Transcriptomic analysis of temporal shifts in berry development between two grapevine cultivars of the Pinot family reveals potential genes controlling ripening time. BMC Plant Biology 21, 327.
| Crossref | Google Scholar |
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7, 562-578.
| Crossref | Google Scholar |
Tyagi S, Shumayla , Sharma Y, Madhu , Sharma A, Pandey A, Singh K, Upadhyay SK (2023) TaGPX1-D overexpression provides salinity and osmotic stress tolerance in Arabidopsis. Plant Science 337, 111881.
| Crossref | Google Scholar |
Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant & Cell Physiology 51, 1821-1839.
| Crossref | Google Scholar |
Vainonen JP, Kangasjärvi J (2015) Plant signalling in acute ozone exposure. Plant, Cell & Environment 38, 240-252.
| Crossref | Google Scholar | PubMed |
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. Journal of Heredity 93, 77-78.
| Crossref | Google Scholar | PubMed |
Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345, 743-746.
| Crossref | Google Scholar | PubMed |
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1-14.
| Crossref | Google Scholar | PubMed |
Wang H, Xiao L, Tong J, Liu F (2010) Foliar application of chlorocholine chloride improves leaf mineral nutrition, antioxidant enzyme activity, and tuber yield of potato (Solanum tuberosum L.). Scientia Horticulturae 125, 521-523.
| Crossref | Google Scholar |
Wang C, Zhao Y, Gu P, Zou F, Meng L, Song W, Yang Y, Wang S, Zhang Y (2018) Auxin is involved in lateral root formation induced by drought stress in tobacco seedlings. Journal of Plant Growth Regulation 37, 539-549.
| Crossref | Google Scholar |
Wang Z-J, Liu H, Zeng F-K, Yang Y-C, Xu D, Zhao Y-C, Liu X, Kaur L, Liu G, Singh J (2023) Potato processing industry in China: current scenario, future trends and global impact. Potato Research 66, 543-562.
| Crossref | Google Scholar | PubMed |
Wassie M, Song S, Cao L, Chen L (2023) A Medicago truncatula calcineurin b-like protein, MtCBL13 confers drought sensitivity in arabidopsis through ABA-dependent pathway. Environmental and Experimental Botany 206, 105141.
| Crossref | Google Scholar |
Watanabe E, Mano S, Hara-Nishimura I, Nishimura M, Yamada K (2017) HSP90 stabilizes auxin receptor TIR1 and ensures plasticity of auxin responses. Plant Signaling & Behavior 12, e1311439.
| Crossref | Google Scholar | PubMed |
Went FW (1928) Wuchsstoff und wachstum. Recueil Des Travaux Botaniques Néerlandais 25, 1-116.
| Google Scholar |
Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S, Robatzek S, Karpiński S, Karpińska B, Kangasjärvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biology 10, 95.
| Crossref | Google Scholar |
Xi Y, Han X, Zhang Z, Joshi J, Borza T, Aqa MM, Zhang B, Yuan H, Wang-Pruski G (2020) Exogenous phosphite application alleviates the adverse effects of heat stress and improves thermotolerance of potato (Solanum tuberosum L.) seedlings. Ecotoxicology and Environmental Safety 190, 110048.
| Crossref | Google Scholar | PubMed |
Xu X, Pan S, Cheng S, Zhang B, Mu D, Ni P, Zhang G, Yang S, Li R, Wang J, Orjeda G, Guzman F, Torres M, Lozano R, Ponce O, Martinez D, De La Cruz G, Chakrabarti SK, Patil VU, Skryabin G, Kuznetsov BB, Ravin NV, Kolganova TV, Beletsky AV, Mardanov AV, Di Genova A, Bolser DM, Martin DMA, Li G, Yang Y, Kuang H, Hu Q, Xiong X, Bishop GJ, Sagredo B, Mejía N, Zagorski W, Gromadka R, Gawor J, Szczesny P, Huang S, Zhang Z, Liang C, He J, Li Y, He Y, Xu J, Zhang Y, Xie B, Du Y, Qu D, Bonierbale M, Ghislain M, Herrera MDR, Giuliano G, Pietrella M, Perrotta G, Facella P, O’Brien K, Feingold SE, Barreiro LE, Massa GA, Diambra L, Whitty BR, Vaillancourt B, Lin H, Massa AN, Geoffroy M, Lundback S, DellaPenna D, Buell CR, Sharma SK, Marshall DF, Waugh R, Bryan GJ, Destefanis M, Nagy I, Milbourne D, Thomson SJ, Fiers M, Jacobs JME, Nielsen KL, Sønderkær M, Iovene M, Torres GA, Jiang J, Veilleux RE, Bachem CWB, De Boer J, Borm T, Kloosterman B, Van Eck H, Datema E, Hekkert BL, Goverse A, Van Ham RCHJ, Visser RGF (2011) Genome sequence and analysis of the tuber crop potato. Nature 475, 465-470.
| Google Scholar |
Yang W, Yang M, Wen H, Jiao Y (2018) Global warming potential of CH4 uptake and N2O emissions in saline–alkaline soils. Atmospheric Environment 191, 172-180.
| Crossref | Google Scholar |
Zameer R, Fatima K, Azeem F, ALgwaiz HIM, Sadaqat M, Rasheed A, Batool R, Shah AN, Zaynab M, Shah AA, Attia KA, AlKahtani MDF, Fiaz S (2022) Genome-wide characterization of superoxide dismutase (SOD) genes in Daucus carota: novel insights into structure, expression, and binding interaction with hydrogen peroxide (H2O2) under abiotic stress condition. Frontiers in Plant Science 13, 870241.
| Crossref | Google Scholar | PubMed |
Zeiner A, Colina FJ, Citterico M, Wrzaczek M (2023) CYSTEINE-RICH RECEPTOR-LIKE PROTEIN KINASES: their evolution, structure, and roles in stress response and development. Journal of Experimental Botany 74, 4910-4927.
| Crossref | Google Scholar |
Zhang W, Ruan J, Ho TD, You Y, Yu T, Quatrano RS (2005) Cis-regulatory element based targeted gene finding: genome-wide identification of abscisic acid-and abiotic stress-responsive genes in Arabidopsis thaliana. Bioinformatics 21, 3074-3081.
| Crossref | Google Scholar | PubMed |
Zhang X, Han X, Shi R, Yang G, Qi L, Wang R, Li G (2013) Arabidopsis cysteine-rich receptor-like kinase 45 positively regulates disease resistance to Pseudomonas syringae. Plant Physiology and Biochemistry 73, 383-391.
| Crossref | Google Scholar | PubMed |
Zhu T, Xin F, Wei S, Liu Y, Han YC, Xie J, Ding Q, Ma L (2019) Genome-wide identification, phylogeny and expression profiling of class III peroxidases gene family in Brachypodium distachyon. Gene 700, 149-162.
| Crossref | Google Scholar | PubMed |
Zuo C, Liu H, Lv Q, Chen Z, Tian Y, Mao J, Chu M, Ma Z, An Z, Chen B (2020) Genome-wide analysis of the apple (Malus domestica) cysteine-rich receptor-like kinase (CRK) family: annotation, genomic organization, and expression profiles in response to fungal infection. Plant Molecular Biology Reporter 38, 14-24.
| Crossref | Google Scholar |
