The Arabidopsis CURVY1 (CVY1) gene encoding a novel receptor-like protein kinase regulates cell morphogenesis, flowering time and seed production
© Gachomo et al.; licensee BioMed Central Ltd. 2014
Received: 14 April 2014
Accepted: 5 August 2014
Published: 27 August 2014
A molecular-level understanding of the loss of CURVY1 (CVY1) gene expression (which encodes a member of the receptor-like protein kinase family) was investigated to gain insights into the mechanisms controlling cell morphogenesis and development in Arabidopsis thaliana.
Using a reverse genetic and cell biology approaches, we demonstrate that CVY1 is a new DISTORTED gene with similar phenotypic characterization to previously characterized ARP2/3 distorted mutants. Compared to the wild type, cvy1 mutant displayed a strong distorted trichome and altered pavement cell phenotypes. In addition, cvy1 null-mutant flowers earlier, grows faster and produces more siliques than WT and the arp2/3 mutants. The CVY1 gene is ubiquitously expressed in all tissues and seems to negatively regulate growth and yield in higher plants.
Our results suggest that CURVY1 gene participates in several biochemical pathways in Arabidopsis thaliana including (i) cell morphogenesis regulation through actin cytoskeleton functional networks, (ii) the transition of vegetative to the reproductive stage and (iii) the production of seeds.
In plants, cell shape patterning and growth are regulated by multiple genes that are mediated by actin and microtubule cytoskeleton-dependent trafficking pathways -. The combined activities of the cytoskeleton, endomembrane, and cell wall biosynthetic systems organize the cytoplasm and define the architectural cell patterning -. Genetic screens have identified a class of mutants known as DISTORTED mutants because of their significant actin-related cytoskeletal growth-associated phenotypic defects and overall distorted cell shape patterning and abnormal polarized growth (trichome, epidermis, cell-cell communication) ,-.
Genetic analysis reveals that gene that function in signal transduction cascades controlling local actin polymerization through the ARP2/3 complex - and the SCAR/WAVE complex ,- regulate cell patterning/morphogenesis in plants. Most of this knowledge comes from studies of differently distorted trichome mutants generally characterized by irregular cell expansion and polarized growth ,,,.
In order to decipher the genetic basis of plant cell shape patterning and growth, we employed, in this study, a reverse genetic approach by screening the loss of gene expressions in Arabidopsis T-DNA knockout mutants to gain insights into the mechanisms controlling cell morphogenesis in plants. DISTORTED mutants are known to display a dramatic cell shape alteration in comparison to wild type plants. The overall cell (trichome, pavement cell, root system) morphology of DISTORTED mutants has been well studied . The DISTORTED genes have been reported to function in signal transduction cascades that control actin cytoskeleton assembly through WAVE/SCAR2-ARP2/3 pathway ,,,.
In this manuscript, we describe a new DISTORTED gene termed CURVY1 (CVY1) that encodes a member of the receptor-like kinase (RLK) superfamily. Protein kinases are generally involved in perception of general elicitors initiating signal transduction cascades regulated by protein phosphorylation  to activate downstream responses that include the production of reactive oxygen species, ethylene biosynthesis, activation of a MAPK cascade, activation of abiotic or defense gene expression and other biological processes -. In addition, RLKs have also been recently related to the regulation of unidimensional cell growth, response to nitrate, and transferase activities in eukaryotes . several protein kinases and their biological phosphorylation processes are still largely uncharacterized in Arabidopsis thaliana. Among the protein kinase genes, the CURVY1 (CVY1) gene appears to have a unique function related to cell morphogenesis, as cvy1 mutant displays phenotypes similar to distorted SCAR/WAVE and ARP2/3 mutant cell morphologies ,,,. Using a reverse genetic approach, we examined and characterized a SALK_T-DNA knockout curvy1 mutant (cvy1) with respect to cell morphogenesis and growth phenotypes. Knockout mutation in CVY1 caused severe trichome growth defects with relatively mild effects on overall shoot development, demonstrating that CVY1 functions in polarized cell growth and cell shape patterning. In addition, the work demonstrates that CURVY1 represents a novel receptor-like kinase that regulates trichome, pavement cell morphogenesis and cell wall biogenesis among other interesting phenotypic features and might function in signal transduction cascades that control local actin assembling through the SCAR2/WAVE-ARP2/3 pathway.
Results and discussion
Genetic and phenotypic characterization of curvy1mutant
Sequences of oligonucleotide primers used in this study
For TDNA insertion
For complementation test (SmaI site italicized)
For complementation test (SmaI site italicized)
Comparative quantitative phenotypic analysis of cvy1 trichomes to well characterized arp2/3 trichome mutants
Branch 1 (μm)
286 ± 31 (n = 16)a
82 ± 27 (n = 10)d
87 ± 31 (n = 14)d
78 ± 26 (n = 12)d
Branch 2 (μm)
256 ± 50 (n = 16)b
30 ± 10 (n = 10)e
29 ± 8 (n = 14)e
28 ± 12 (n = 12)e
Branch 3 (μm)
196 ± 46 (n = 16)c
22 ± 12 (n = 10)f
18 ± 7 (n = 14)f
20 ± 8 (n = 12)f
Comparative quantitative analysis of cvy1 pavement cell shape phenotype to well characterized arp2/3 pavement cells
2.10 ± 0.6 (n = 25)a
1.56 ± 0.3 (n = 24)d
1.70 ± 0.61 (n = 20)d
1.62 ± 0.31 (n = 28)d
0.25 ± 0.06 (n = 25)a
0.38 ± 0.05 (n = 24)d
0.34 ± 0.06 (n = 20)d
0.30 ± 0.03 (n = 28)d
CURVY1 controls cell morphogenesis in plants
Overexpression of CVY1 gene rescues the overall cvy1 phenotypes in complementation tests
Flowering time (in number of rosette leaves)
14.0 ± 1.5 (n = 22)a
10.0 ± 1.1 (n = 28)b
15.5 ± 2.0 (n = 12)a
Number of siliques/seed production at 31 days
12.5 ± 2.0 (n = 22)a
45.0 ± 5.0 (n = 28)b
14.0 ± 4.0 (n = 12)a
Dark grown phenotype
GG (n = 22)
LGG (n = 28)
GG (n = 12)
The effect of latrunculin B (LatB) on wild type arp2/3 and cvy1 seedlings
Root length (mm)
15.5 ± 0.5 (n = 22)a
15.0 ± 0.3 (n = 28)a
10.0 ± 0.6 (n = 12)b
9.0 ± 0.3 (n = 12)b
LatB (5 nM)
7.0 ± 0.05 (n = 22)c
5.0 ± 0.05 (n = 28)d
4.5 ± 0.06 (n = 12)d
4.0 ± 0.03 (n = 12)d
CURVY1encodes a member of the receptor-like kinase (RLK) protein family
The RLKs are integral plasma membrane associated proteins with an extracellular domain that mainly binds to a carbohydrate, a transmembrane domain, and an intracellular Ser/Thr kinase domain . Overall, plant RLKs have been reported to regulate various signaling pathways, including meristem function, brassinosteroid perception, floral abscission, ovule development and embryogenesis, plant defense, and plant morphology . Previous studies showed that selected members of Arabidopsis CrRLK gene family including FERONIA (FER: At3g51550) -, THESEUS1 (THE1: At5g54380) , HERCULES1 , ANXUR1 and ANXUR2 (ANX1 and ANX2) , regulate cell growth processes in different tissues under different development conditions. Likewise, CURVY1 has been found to control plant cell morphology and overall growth including flowering time, cell polarity, and actin cytoskeleton network.
Actin bundles are disorganized in curvy1epidermal cells
CURVY1controls other biological processes in plants
In summary, we present in this work the identification of a new gene, CURVY1 that regulates growth, cell morphogenesis and seed production in Arabidopsis thaliana. This work presents evidence that CURVY1 belongs to the “distorted group” of genes. Homozygous cvy1 mutant displayed strong morphological phenotypes that are indistinguishable from the well-characterized DISTORTED trichome mutants . The CURVY1 gene encoding a receptor-like protein kinase is ubiquitously expressed in all tissues tested. The distorted trichome phenotype in cvy1 mutant was rescued by expressing CURVY1 gene in the mutant background. Unlike the other DISTORTED mutants, mutation of CURVY1 gene promotes early flowering and seed production in Arabidopsis thaliana. Overall, CURVY1 represents a novel receptor-like kinase gene involved in regulating cell morphogenesis, including trichome and pavement cell shape patterning through local actin cytoskeleton assembling and additionally functions in signal transduction cascades that control flowering time and seed production in plants.
Plant strain, growth conditions and mutant characterization
Arabidopsis thaliana (ecotype Col-0) and cvyt1 knockout mutant (T-DNA SALK_018797) [from Arabidopsis Biological Research Center (ABRC)] were used throughout this work. Appropriate seeds were sown on Murashige and Skoog (1× MS) agar plates or soil and seedlings were allowed to grow under continuous illumination (120–150 μEm−2 s−1) at 24°C. For cvy1 mutant characterization, T-DNA insertion was PCR-confirmed using CVY1 gene specific primers (Table 1) and T-DNA left border primer Lb (Table 1). To analyze the expression of CVY1 gene in mutant backgrounds, total RNA was extracted from the homozygous T-DNA insertion mutants by TRIzol reagent (Molecular Research Center) and then reversed transcribed using qScript cDNA Supermix (Quanta BioSciences, Gaithersburg, MD, USA) as previously described . Thereafter, the cDNA was used as template for PCR using CVY1 gene-specific primers (Table 1), running 30 amplification cycles (linear range of amplification) . PCR fragments were separated on 1% agarose gels containing ethidium bromide. A cDNA fragment generated from ACTIN served as an internal control.
For complementation test, a RT-PCR amplification of 2600 bp fragment containing the 5’ and 3’ untranslated regions as well as CVY1-encoding sequence (At2g39360) from WT cDNA (Table 1) was cloned into the SmaI site of the pROK2 vector  in front of CaMV 35S promoter-driven overexpression , and stably transformed cvy1 mutant background by the floral dip method . For tissue specific gene expression analysis, the cDNA from respective tissues was used to perform real-time qPCR of CVY1 gene expression. Real-time qPCR was performed on Eco real-time PCR system (Illumina, San Diego, CA, USA) using PerfeCTa SYBR green FastMix (Quanta BioScience, Gaithersburg, MD, USA). The relative CVY1 expression level was assessed using ACTIN gene as internal control (Table 1).
Arabidopsis thalianaCrRLK1-like family: structural characterization and phylogenetic analysis
Catharanthus roseus RLK (CrRLK) characteristics were used to retrieve the 17 members of Arabidopsis thaliana CrRLK1-like gene family according to Hematy and Hofte  and used to generate the phylogenetic tree according to Gachomo et al. . CURVY1 (a member of CrRLK1-like family) protein functional domains were studied using different structure-functional motifs and/or patterns databases such as Pfam v25.0 (pfam.sanger.ac.uk), Prosite (prosite.expasy.org/scanprosite) and Conserved Domain Database (CDD) v3.02, CDART (Conserved Domain Architecture Retrieval Tool) to reveal the kinase catalytic domains, the carbohydrate, substrate and ATP binding sites and their 3D structural features according to Gachomo et al. .
Scanning electron microscopy (SEM)
SEM images of upper developing leaves, showing mature trichomes of WT and cvy1 mutant were acquired at different magnifications as previously described . SEM images were taken using a LEO 1450 EP SEM .
Cell morphological analysis
Confocal image analysis was performed on one week after germination of plate grown plants. Pavement-cell shape analysis was performed by staining the samples with 10 μM of the lipophilic dye, FM464, for 2 hr in darkness under rocking conditions. The images were acquired using confocal microscopy (inverted Leica SP8 confocal microscope at 488 nm, 25% laser power and emission at 600 nm). The F-actin localization was done according to Kotchoni et al. . Images were collected using an inverted Leica SP8 confocal microscope with water-immersion objective. The images were processed and analyzed using ImageJ software.
Determination of flowering time
Flowering time was assessed by counting the number of rosette leaves when flower bolts were 1 cm in length or when floral buds were visible at the center of the rosette as previously reported ,.
Experiments were performed at least three times. Data were expressed as mean values ± SE. P values were determined by Student’s t test analysis.
We acknowledged the NSF DBI-0216233 MRI grant “Acquisition of a Scanning Electron Microscope for Collaborative Use at Rutgers, Camden” for the acquisition of the Arabidopsis SEM images in this work. This work was supported by NSF-REU DBI # 1263163 grant and Rutgers-University start-up funds to SOK.
- Geitmann A: Mechanical modeling and structural analysis of the primary plant cell wall. Curr Opi Plant Biol. 2010, 13: 693-699. 10.1016/j.pbi.2010.09.017.View ArticleGoogle Scholar
- Kotchoni SO, Zakharova T, Mallery EL, El-Din El-Assal S, Le J, Szymanski DB: The association of the Arabidopsis actin-related protein (ARP) 2/3 complex with cell membranes is linked to its assembly status, but not to its activation. Plant Physiol. 2009, 151: 2095-2109. 10.1104/pp.109.143859.PubMed CentralView ArticlePubMedGoogle Scholar
- Zhang C, Kotchoni SO, Samuels L, Szymanski DB: SPIKE1 signals originate from and assemble specialized domains of the endoplasmic reticulum. Curr Biol. 2010, 20: 2144-2149. 10.1016/j.cub.2010.11.016.View ArticlePubMedGoogle Scholar
- Hulskamp M, Misera S, Jurgens G: Genetic dissection of trichome cell development in Arabidopsis. Cell. 1994, 76: 555-566. 10.1016/0092-8674(94)90118-X.View ArticlePubMedGoogle Scholar
- Uhrig JF, Mutondo M, Zimmermann I, Deeks MJ, Machesky LM, Thomas P, Uhrig S, Rambke C, Hussey PJ, Hulskamp M: The role of Arabidopsis SCAR genes in ARP2–ARP3-dependent cell morphogenesis. Development. 2007, 134: 967-977. 10.1242/dev.02792.View ArticlePubMedGoogle Scholar
- Zhang C, Mallery E, Reagan S, Boyko VP, Kotchoni SO, Szymanski DB: The endoplasmic reticulum is a reservoir for WAVE/SCAR regulatory complex signaling in the Arabidopsis leaf. Plant Physiol. 2013, 162: 689-706. 10.1104/pp.113.217422.PubMed CentralView ArticlePubMedGoogle Scholar
- Mathur J: The ARP2/3 complex: giving plant cells a leading edge. Bioessays. 2005, 27: 377-387. 10.1002/bies.20206.View ArticlePubMedGoogle Scholar
- Smith LG, Oppenheimer DG: Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol. 2005, 21: 271-295. 10.1146/annurev.cellbio.21.122303.114901.View ArticlePubMedGoogle Scholar
- Szymanski DB: Breaking the WAVE complex: the point of Arabidopsis trichomes. Curr Opin Plant Biol. 2005, 8: 103-112. 10.1016/j.pbi.2004.11.004.View ArticlePubMedGoogle Scholar
- Hussey PJ, Ketelaar T, Deeks MJ: Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Biol. 2006, 57: 109-125. 10.1146/annurev.arplant.57.032905.105206.View ArticlePubMedGoogle Scholar
- Basu D, El-Assal Sel D, Le J, Mallery EL, Szymanski DB: Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRA1 during leaf epidermal development. Development. 2004, 131: 4345-4355. 10.1242/dev.01307.View ArticlePubMedGoogle Scholar
- Brembu T, Winge P, Seem M, Bones AM: NAPP and PIRP encode subunits of a putative wave regulatory protein complex involved in plant cell morphogenesis. Plant Cell. 2004, 16: 2335-2349. 10.1105/tpc.104.023739.PubMed CentralView ArticlePubMedGoogle Scholar
- Deeks MJ, Kaloriti D, Davies B, Malho R, Hussey PJ: Arabidopsis NAP1 is essential for Arp2/3-dependent trichome morphogenesis. Curr Biol. 2004, 14: 1410-1414. 10.1016/j.cub.2004.06.065.View ArticlePubMedGoogle Scholar
- Frank M, Egile C, Dyachok J, Djakovic S, Nolasco M, Li R, Smith LG: Activation of Arp2/3 complex-dependent actin polymerization by plant proteins distantly related to Scar/WAVE. Proc Natl Acad Sci USA. 2004, 101: 16379-16384. 10.1073/pnas.0407392101.PubMed CentralView ArticlePubMedGoogle Scholar
- Saedler R, Zimmermann I, Mutondo M, Hulskamp M: The Arabidopsis KLUNKER gene controls cell shape changes and encodes the AtSRA1 homolog. Plant Mol Biol. 2004, 56: 775-782. 10.1007/s11103-004-4951-z.View ArticlePubMedGoogle Scholar
- Zimmermann I, Saedler R, Mutondo M, Hulskamp M: The Arabidopsis GNARLED gene encodes the NAP125 homolog and controls several actin-based cell shape changes. Mol Genet Genomics. 2004, 272: 290-296. 10.1007/s00438-004-1052-2.View ArticlePubMedGoogle Scholar
- Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG: IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell. 2005, 17: 2314-2326. 10.1105/tpc.104.028670.PubMed CentralView ArticlePubMedGoogle Scholar
- Le J, Mallery EL, Zhang C, Brankle S, Szymanski DB: Arabidopsis BRICK1/HSPC300 is an essential WAVE-complex subunit that selectively stabilizes the Arp2/3 activator SCAR2. Curr Biol. 2006, 16: 895-901. 10.1016/j.cub.2006.03.061.View ArticlePubMedGoogle Scholar
- Schwab B, Folkers U, Ilgenfritz H, Hulskamp M: Trichome morphogenesis in Arabidopsis. Philos Trans R Soc Lond B Biol Sci. 2000, 355: 879-883. 10.1098/rstb.2000.0623.PubMed CentralView ArticlePubMedGoogle Scholar
- Zhang C, Mallery EL, Schlueter J, Huang S, Fan Y, Brankle S, Staiger CJ, Szymanski DB: Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis. Plant Cell. 2008, 20: 995-1011. 10.1105/tpc.107.055350.PubMed CentralView ArticlePubMedGoogle Scholar
- Szymanski DB: Plant cells taking shape: new insights into cytoplasmic control. Curr Opin Plant Biol. 2009, 12: 735-744. 10.1016/j.pbi.2009.10.005.View ArticlePubMedGoogle Scholar
- Benschop JJ, Mohammed S, O’Flaherty M, Heck AJR, Slijper M, Menke FLH: Quantitative Phosphoproteomics of Early Elicitor Signaling in Arabidopsis. Mol Cell Proteomics. 2007, 6: 1198-1214. 10.1074/mcp.M600429-MCP200.View ArticlePubMedGoogle Scholar
- Gomez-Gomez L, Felix G, Boller T: A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 1999, 18: 277-284. 10.1046/j.1365-313X.1999.00451.x.View ArticlePubMedGoogle Scholar
- Nuhse TS, Peck SC, Hirt H, Boller T: Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. J Biol Chem. 2000, 275: 7521-7526. 10.1074/jbc.275.11.7521.View ArticlePubMedGoogle Scholar
- Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J: MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. 2002, 415: 977-983. 10.1038/415977a.View ArticlePubMedGoogle Scholar
- Kotchoni SO, Gachomo EW: The reactive oxygen species network pathways: an essential prerequisite for perception of pathogen attack and disease resistance in plants. J Biosci. 2006, 31: 389-404. 10.1007/BF02704112.View ArticlePubMedGoogle Scholar
- Schwab B, Mathur J, Saedler R, Schwarz H, Frey B, Scheidegger C, Hulskamp M: Regulation of cell expansion by the DISTORTED genes in Arabidopsis thaliana: actin controls the spatial organization of microtubules. Mol Genet Genomics. 2003, 269: 350-360. 10.1007/s00438-003-0843-1.View ArticlePubMedGoogle Scholar
- Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W: GENEVESTIGATOR: Arabidopsis microarray database and analysis toolbox. Plant Physiol. 2004, 136: 2621-2632. 10.1104/pp.104.046367.PubMed CentralView ArticlePubMedGoogle Scholar
- Clough SJ, Bent AF: Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998, 16: 735-743. 10.1046/j.1365-313x.1998.00343.x.View ArticlePubMedGoogle Scholar
- Gachomo EW, Jimenez-Lopez JC, Jno Baptiste L, Kotchoni SO: GIGANTUS1 (GTS1), a member of Transducin/WD40 protein superfamily, controls seed germination, growth and biomass accumulation through ribosome-biogenesis protein interactions in Arabidopsis thaliana. BMC Plant Biol. 2014, 14: 37-10.1186/1471-2229-14-37.PubMed CentralView ArticlePubMedGoogle Scholar
- Steinwand BJ, Kieber JJ: The role of receptor-like kinases in regulating cell wall function. Plant Physiol. 2010, 153: 479-484. 10.1104/pp.110.155887.PubMed CentralView ArticlePubMedGoogle Scholar
- Becraft PW: Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol. 2002, 18: 163-192. 10.1146/annurev.cellbio.18.012502.083431.View ArticlePubMedGoogle Scholar
- Huck N, Moore JM, Federer M, Grossniklaus U: The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development. 2003, 130: 2149-2159. 10.1242/dev.00458.View ArticlePubMedGoogle Scholar
- Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure JE: Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol. 2003, 13: 432-436. 10.1016/S0960-9822(03)00093-9.View ArticlePubMedGoogle Scholar
- Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y: Three related receptorlike kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2009, 106: 7648-7653. 10.1073/pnas.0812346106.PubMed CentralView ArticlePubMedGoogle Scholar
- Deslauriers SD, Larsen PB: FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol Plant. 2010, 3: 626-640. 10.1093/mp/ssq015.View ArticlePubMedGoogle Scholar
- Hematy K, Sado PE, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou JP, Hofte H: A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol. 2007, 17: 922-931. 10.1016/j.cub.2007.05.018.View ArticlePubMedGoogle Scholar
- Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U: Disruption of the pollenexpressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development. 2009, 136: 3279-3288. 10.1242/dev.040071.PubMed CentralView ArticlePubMedGoogle Scholar
- Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M: ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol. 2009, 19: 1327-1331. 10.1016/j.cub.2009.06.064.View ArticlePubMedGoogle Scholar
- Hematy K, Hofte H: Novel receptor kinases involved in growth regulation. Curr Opi Plant Biol. 2008, 11: 321-328. 10.1016/j.pbi.2008.02.008.View ArticleGoogle Scholar
- Lindner H, Muller LM, Boisson-Dernier A, Grossniklaus U: CrRLK1L receptor-like kinases: not just another brick in the wall. Curr Opi Plant Biol. 2012, 15: 659-669. 10.1016/j.pbi.2012.07.003.View ArticleGoogle Scholar
- Shiu SH, Bleecker AB: Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA. 2001, 98: 10763-10768. 10.1073/pnas.181141598.PubMed CentralView ArticlePubMedGoogle Scholar
- Kotchoni SO, Kuhns C, Ditzer A, Kirch H-H, Bartels D: Over-expression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ. 2006, 29: 1033-1048. 10.1111/j.1365-3040.2005.01458.x.View ArticlePubMedGoogle Scholar
- Baulcombe DC, Saunders GS, Bevan MW, Mayo MA, Harrison BD: Expression of biologically active viral satellite RNA from the nuclear genome of transformed plants. Nature. 1986, 321: 446-449. 10.1038/321446a0.View ArticleGoogle Scholar
- Kotchoni SO, Larrimore KE, Mukherjee M, Kempinski CF, Barth C: Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis. Plant Physiol. 2009, 149: 803-815. 10.1104/pp.108.132324.PubMed CentralView ArticlePubMedGoogle Scholar
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