Isolation and characterisation of six putative wheat cell wall-associated kinases
Yong Liu A B D , Dongcheng Liu A , Haiying Zhang A B , Hongbo Gao C , Xiaoli Guo C , Xiangdong Fu A and Aimin Zhang A EA State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
B Graduate School of the Chinese Academy of Sciences, Beijing 100101, China.
C China Agricultural University, Beijing 100094, China.
D Current address: Department of Physiology, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI 53226, USA.
E Corresponding author. Email: amzhang@genetics.ac.cn
Functional Plant Biology 33(9) 811-821 https://doi.org/10.1071/FP06041
Submitted: 27 February 2006 Accepted: 19 May 2006 Published: 1 September 2006
Abstract
The plant cell wall-associated kinase (WAK) and WAK-like kinase (WAKL) make up a unique group in the receptor-like protein kinase (RLK) superfamily. Previous studies on Arabidopsis have revealed that the WAK gene family members play an important role in both cell elongation and stress response signalling. Here we show that four putative WAKs (TaWAK1, TaWAKL2, TaWAKL3, and TaWAK4) and two WAKLs (TaWAKL1 and TaWAKL2) were isolated from wheat based on the DNA sequence similarity and the protein structure conservation of Arabidopsis WAKs genes. TaWAK1, TaWAK2, TaWAK3 and TaWAKL1 each encode a putative intact protein with the characteristic of the WAK / WAKL gene family members, except for the abbreviated TaWAK4 and TaWAKL2 which were caused by nucleotide mutation and alternative splicing, respectively. Southern analysis revealed that TaWAKL1, TaWAK1, TaWAK2 and TaWAK3 are all multiple-copy members. Real-time PCR analysis revealed that the TaWAK1 and TaWAK3 displayed similar expression patterns, while expressions of TaWAKL1, TaWAKL2, and TaWAK2 were organ specific. Further, we analysed the conservation of introns and intron–exon structure and the putative protein structures between wheat and Arabidopsis, which showed the putative wheat WAKs are different from those of Arabidopsis and make up a new subgroup in the polygenetic tree.
Keywords: cell wall-associated kinase, gene, WAK, wheat.
Acknowledgments
We thank SW Wang (Jiangsu Academy of Agricultural Sciences) for providing the dwarf wheat line Ning 982105. We also thank Douglas D Archbold (University of Kentucky) and Jennifer L Pietruze (Medical College of Wisconsin) for critical review of the manuscript. This work was supported by the National Natural Science Foundation of China (30521001, 30025031) and the Chinese Academy of Sciences program (KSCX2-SW-304) with grants to A Zhang.
Anderson CM,
Wagner TA,
Perret M,
He ZH,
He D, Kohorn BD
(2001) WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Molecular Biology 47, 197–206.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Artavanis-Tsakonas S,
Matsuno K, Fortini ME
(1995) Notch signaling. Science 268, 225–232.
| PubMed |
Artavanis-Tsakonas S,
Rand MD, Lake RJ
(1999) Notch signaling: cell fate control and signal integration in development. Science 284, 770–776.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Banner DW,
D’Arcy A,
Chene C,
Winkler FK,
Guha A,
Konigsberg WH,
Nemerson Y, Kirchhofer D
(1996) The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 380, 41–46.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Becraft PW
(1998) Receptor kinases in plant development. Trends in Plant Science 3, 384–388.
| Crossref | GoogleScholarGoogle Scholar |
Becraft PW
(2002) Receptor kinase signaling in plant development. Annual Review of Cell and Developmental Biology 18, 163–192.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Blasi F,
Vassalli JD, Dano K
(1987) Urokinase-type plasminogen activator: proenzyme, receptor, and inhibitors. Journal of Cell Biology 104, 801–804.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cosgrove DJ
(2001) Plant cell walls: wall-associated kinases and cell expansion. Current Biology 11, R558–R559.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Davis CG
(1990) The many faces of epidermal growth factor repeats. The New Biologist 2, 410–419.
| PubMed |
Decreux A, Messiaen J
(2005) Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant & Cell Physiology 46, 268–278.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Edgington TS,
Dickinson CD, Ruf W
(1997) The structural basis of function of the TF VIIa complex in the cellular initiation of coagulation. Thrombosis and Haemostasis 78, 401–405.
| PubMed |
Ellis MH,
Rebetzke GJ,
Chandler P,
Bonnett D,
Spielmeyer W, Richards RA
(2004) The effect of different height reducing genes on the early growth of wheat. Functional Plant Biology 31, 583–589.
| Crossref | GoogleScholarGoogle Scholar |
Fedorov A,
Fedorova L,
Starshenko V,
Filatov V, Grigor’ev E
(1998) Influence of exon duplication on intron and exon phase distribution. Journal of Molecular Evolution 46, 263–271.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fulton TM,
Chunwongse J, Tanksley SD
(1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Molecular Biology Reporter 13, 207–209.
Gens JS,
Fujiki M, Pickard BG
(2000) Arabinogalactan protein and wall-associated kinase in a plasmalemmal reticulum with specialized vertices. Protoplasma 212, 115–134.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Haffani YZ,
Silva NF, Goring DR
(2004) Receptor kinase signalling in plants. Canadian Journal of Botany 82, 1–15.
| Crossref | GoogleScholarGoogle Scholar |
He ZH,
Fujiki M, Kohorn BD
(1996) A cell wall-associated, receptor-like protein kinase. Journal of Biological Chemistry 271, 19 789–19 793.
| Crossref | GoogleScholarGoogle Scholar |
He ZH,
He D, Kohorn BD
(1998) Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. The Plant Journal 14, 55–63.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
He ZH,
Cheeseman I,
He D, Kohorn BD
(1999) A cluster of five cell wall-associated receptor kinase genes, WAK1–5, are expressed in specific organs of Arabidopsis. Plant Molecular Biology 39, 1189–1196.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kohorn BD
(2001) WAKs: cell wall associated kinases. Current Opinion in Cell Biology 13, 529–533.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lally D,
Ingmire P,
Tong HY, He ZH
(2001) Antisense expression of a cell wall-associated protein kinase, WAK4, inhibits cell elongation and alters morphology. The Plant Cell 13, 1317–1331.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lee Y, Kende H
(2001) Expression of β-expansins is correlated with internodal elongation in deepwater rice. Plant Physiology 127, 645–654.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Letunic I,
Copley RR,
Schmidt S,
Ciccarelli FD,
Doerks T,
Schultz J,
Ponting CP, Bork P
(2004) SMART 40: towards genomic data integration. Nucleic Acids Research 32, D142–D144.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ling HQ,
Zhu Y, Keller B
(2003) High-resolution mapping of the leaf rust disease resistance gene Lr1 in wheat and characterization of BAC clones from the Lr1 locus. Theoretical and Applied Genetics 106, 875–882.
| PubMed |
Long M,
Rosenberg C, Gilbert W
(1995) Intron phase correlations and the evolution of the intron / exon structure of genes. Proceedings of the National Academy of Sciences USA 92, 12 495–12 499.
Maleck K,
Levine A,
Eulgem T,
Morgan A,
Schmid J,
Lawton KA,
Dangl JL, Dietrich RA
(2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genetics 26, 403–410.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Morris ER, Walker JC
(2003) Receptor-like protein kinases: the keys to response. Current Opinion in Plant Biology 6, 339–342.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nakai K, Kanehisa M
(1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14, 897–911.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Park AR,
Cho SK,
Yun UJ,
Jin MY,
Lee SH,
Sachetto-Martins G, Park OK
(2001) Interaction of the Arabidopsis receptor protein kinase WAK1 with a glycine-rich protein, AtGRP-3. Journal of Biological Chemistry 276, 26 688–26 693.
| Crossref | GoogleScholarGoogle Scholar |
Patthy L
(1987) Intron-dependent evolution: preferred types of exons and introns. FEBS Letters 214, 1–7.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schenk PM,
Kazan K,
Wilson I,
Anderson JR,
Richmond T,
Somerville SC, Manners JM
(2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences USA 97, 11 655–11 660.
| Crossref | GoogleScholarGoogle Scholar |
Schultz J,
Milpetz F,
Bork P, Ponting CP
(1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences USA 95, 5857–5864.
| Crossref | GoogleScholarGoogle Scholar |
Sivaguru M,
Ezaki B,
He ZH,
Tong H,
Osawa H,
Baluska F,
Volkmann D, Matsumoto H
(2003) Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiology 132, 2256–2266.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stenflo J,
Stenberg Y, Muranyi A
(2000) Calcium-binding EGF-like modules in coagulation proteinases: function of the calcium ion in module interactions. Biochimica et Biophysica Acta 1477, 51–63.
| PubMed |
Verica JA, He ZH
(2002) The cell wall-associated kinase (WAK) and WAK-like kinase gene family. Plant Physiology 129, 455–459.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Verica JA,
Chae L,
Tong H,
Ingmire P, He ZH
(2003) Tissue-specific and developmentally regulated expression of a cluster of tandemly arrayed cell wall-associated kinase-like kinase genes in Arabidopsis. Plant Physiology 133, 1732–1746.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Villadsen D,
Rung JH, Nielsen TN
(2005) Osmotic stress changes carbohydrate partitioning and fructose-2,6-bisphosphate metabolism in barley leaves. Functional Plant Biology 32, 1033–1043.
| Crossref | GoogleScholarGoogle Scholar |
Wagner TA, Kohorn BD
(2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. The Plant Cell 13, 303–318.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhang S,
Chen C,
Li L,
Meng L,
Singh J,
Jiang N,
Deng XW,
He ZH, Lemaux PG
(2005) Evolutionary expansion, gene structure, and expression of the rice wall-associated kinase gene family. Plant Physiology 139, 1107–1124.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
