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.
KeywordsCURVY1 Cell morphogenesis Arabidopsis thaliana Distorted trichome T-DNA knockout mutant Actin bundle Protein kinase Seed production
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.
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