Planta

, Volume 241, Issue 3, pp 603–613 | Cite as

Genome-wide identification and analysis of Catharanthus roseus RLK1-like kinases in rice

  • Quynh-Nga Nguyen
  • Yang-Seok Lee
  • Lae-Hyeon Cho
  • Hee-Jeong Jeong
  • Gynheung An
  • Ki-Hong Jung
Original Article

Abstract

Main conclusion

A genome-wide survey ofCatharanthus roseusreceptor-like kinase1-like kinases (CrRLK1Ls) in rice revealed that the pattern of expression by some CrRLK1Ls is controlled by drought or circadian rhythms. This is probably accomplished through the functioning ofGigantea(OsGI). Such findings provide a novel angle for using CrRLK1Ls to study the drought-stress response and circadian regulation.

Abstract

The 17 CrRLK1L members of a novel RLK family have been identified in Arabidopsis. Each carries a putative extracellular carbohydrate-binding malectin-like domain. However, their roles in rice, a widely consumed staple food, are not well understood. To investigate the functions of CrRLK1Ls in rice, we utilized phylogenomics data obtained through anatomical and diurnal meta-expression analyses. This information was integrated with a large set of public microarray data within the context of the rice CrRLK1L family phylogenic tree. Chromosomal locations indicated that 3 of 16 genes were tandem-duplicated, suggesting possible functional redundancy within this family. However, integrated diurnal expression showed functional divergence between two of three genes, i.e., peak expression was detected during the day for OsCrRLK1L2, but during the night for OsCrRLK1L3. We found it interesting that OsCrRLK1L2 expression was repressed in osgigantea (osgi) mutants, which suggests that it could function downstream of OsGI. Network analysis associated with OsCrRLK1L2 and OsGI suggested a novel circadian regulation mechanism mediated by OsGI. In addition, two of five OsCrRLK1Ls preferentially expressed in the roots were stimulated by drought, suggesting a potential role for this family in water-use efficiency. This preliminary identification of CrRLK1Ls and study of their expression in rice will facilitate further functional classifications and applications in plant production.

Keywords

Circadian regulation CrRLK1L family GIGANTEA Meta-profiling analysis Rice 

Abbreviations

DAT

Days after treatment

GO

Gene ontology

RGAP

Rice Genome Annotation Project

RLK

Receptor-like kinase

TAIR

The Arabidopsis Information Resource

Supplementary material

425_2014_2203_MOESM1_ESM.jpg (862 kb)
Supplementary material 1 Fig. S1 CrRLK1L mapping on rice chromosomes. Red box indicates tandem-duplicated genes. Chromosome numbers are shown at top of each bar. (JPEG 862 kb)
425_2014_2203_MOESM2_ESM.jpg (1.3 mb)
Supplementary material 2 Fig. S2 CrRLK1L rice family phylogenomics with GO and ortholog information in Arabidopsis. Each Locus id and gene name is defined from RGAP. Pale-orange box, Group I; pale-green box,Group II; pale-yellow box, Group III. (JPEG 1373 kb)
425_2014_2203_MOESM3_ESM.jpg (1.2 mb)
Supplementary material 3 Fig. S3 Circadian expression of 17 Arabidopsis CrRLK1L members. Heat map was generated using Affymetrix Arabidopsis ATH1 genome array data sets (GSE3416) that contain expression information from 3 biological replicates of diurnal time series (4-h intervals for 24 h). Yellow, high expression; blue, low expression. (JPEG 1212 kb)
425_2014_2203_MOESM4_ESM.jpg (3.2 mb)
Supplementary material 4 Fig. S4 Effect of drought stress on morphology of WT rice. Plants were initially well-watered for 30 d, then exposed to either water-deficit or control (well-watered) conditions for 3 or 4 d. Length of white bar = 5 cm. (JPEG 3229 kb)
425_2014_2203_MOESM5_ESM.jpg (1.7 mb)
Supplementary material 5 Fig. S5 Primary structures of Arabidopsis and rice CrRLK1L family members. Proteins contain extracellular carbohydrate-binding malectin-like domain(s) (red box) and transmembrane domain (yellow box), plus protein kinase domain (blue box) that shares catalytic functions found in serine/threonine-protein kinases, tyrosine-protein kinases, and dual-specificity protein kinases. (JPEG 1772 kb)
425_2014_2203_MOESM6_ESM.docx (21 kb)
Supplementary material 6 Table S1 Detailed information for rice CrRLK1L family members. (DOCX 21 kb)
425_2014_2203_MOESM7_ESM.docx (22 kb)
Supplementary material 7 Table S2 Primer sequences used for RT-PCR and real-time PCR analyses. (DOCX 22 kb)

References

  1. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM (2011) NCBI GEO: archive for functional genomics data sets—10 years on. Nucleic Acids Res 39:D1005–D1010CrossRefPubMedCentralPubMedGoogle Scholar
  2. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  3. Boisson-Dernier A, Kessler SA, Grossniklaus U (2011) The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals. J Exp Bot 62:1581–1591CrossRefPubMedGoogle Scholar
  4. Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol 11:e1001719    CrossRefPubMedCentralPubMedGoogle Scholar
  5. Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U (2009) Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136:3279–3288CrossRefPubMedCentralPubMedGoogle Scholar
  6. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193CrossRefPubMedGoogle Scholar
  7. Botstein D, Cherry J, Ashburner M, Ball C, Blake J, Butler H, Davis A, Dolinski K, Dwight S, Eppig J (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29CrossRefPubMedCentralPubMedGoogle Scholar
  8. Cao P, Jung K-H, Choi D, Hwang D, Zhu J, Ronald PC (2012) The rice oligonucleotide array database: an atlas of rice gene expression. Rice 5:1–9CrossRefGoogle Scholar
  9. Chandran AKN, Jung KH (2014) Resources for systems biology in rice. J Plant Biol 57:80–92CrossRefGoogle Scholar
  10. Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482CrossRefPubMedGoogle Scholar
  11. Cheung AY, Wu HM (2011) THESEUS 1, FERONIA and relatives: a family of cell wall-sensing receptor kinases? Curr Opin Plant Biol 14:632–641CrossRefPubMedGoogle Scholar
  12. Conte MG, Gaillard S, Droc G, Perin C (2008a) Phylogenomics of plant genomes: a methodology for genome-wide searches for orthologs in plants. BMC Genom 9:183CrossRefGoogle Scholar
  13. Conte MG, Gaillard S, Lanau N, Rouard M, Périn C (2008b) GreenPhylDB: a database for plant comparative genomics. Nuc Acids Res 36:D991–D998CrossRefGoogle Scholar
  14. Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936CrossRefPubMedCentralPubMedGoogle Scholar
  15. Duan Q, Kita D, Li C, Cheung AY, Wu HM (2010) FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Nat Acad Sci USA 107:17821–17826CrossRefPubMedCentralPubMedGoogle Scholar
  16. Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L, Wu H-M, Cheung AY (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun 5:3129PubMedGoogle Scholar
  17. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–660CrossRefPubMedGoogle Scholar
  18. Farooq M, Wahid A, Lee D-J, Ito O, Siddique KH (2009) Advances in drought resistance of rice. Crit Rev Plant Sci 28:199–217CrossRefGoogle Scholar
  19. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J (1999) GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18:4679–4688CrossRefPubMedCentralPubMedGoogle Scholar
  20. Fukao T, Xiong L (2013) Genetic mechanisms conferring adaptation to submergence and drought in rice: simple or complex? Currt Opin Plant Biol 16:196–204CrossRefGoogle Scholar
  21. Goyal K, Walton L, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157CrossRefPubMedCentralPubMedGoogle Scholar
  22. Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y (2009a) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Nat Acad Sci USA 106:7648–7653CrossRefPubMedCentralPubMedGoogle Scholar
  23. Guo H, Ye H, Li L, Yin Y (2009b) A family of receptor-like kinases are regulated by BES1 and involved in plant growth in Arabidopsis thaliana. Plant Sign Behav 4:784–786CrossRefGoogle Scholar
  24. Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–411CrossRefPubMedGoogle Scholar
  25. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–722CrossRefPubMedGoogle Scholar
  26. Hématy K, Sado P-E, van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou J-P, Höfte H (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17:922–931CrossRefPubMedGoogle Scholar
  27. Itoh H, Izawa T (2011) A study of phytohormone biosynthetic gene expression using a circadian clock-related mutant in rice. Plant Sign Behav 6:1932–1936CrossRefGoogle Scholar
  28. Izawa T (2012) Physiological significance of the plant circadian clock in natural field conditions. Plant Cell Environ 35:1729–1741CrossRefPubMedGoogle Scholar
  29. Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6:113–120CrossRefPubMedGoogle Scholar
  30. Izawa T, Mihara M, Suzuki Y, Gupta M, Itoh H, Nagano AJ, Motoyama R, Sawada Y, Yano M, Hirai MY, Makino A, Nagamura Y (2011) Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. Plant Cell 23:1741–1755CrossRefPubMedCentralPubMedGoogle Scholar
  31. Jung KH, Gho HJ, Nguyen MX, Kim SR, An G (2013) Genome-wide expression analysis of HSP70 family genes in rice and identification of a cytosolic HSP70 gene highly induced under heat stress. Funct Integr Gen 13:391–402CrossRefGoogle Scholar
  32. Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330:968–971CrossRefPubMedGoogle Scholar
  33. Kim WY, Ali Z, Park HJ, Park SJ, Cha JY, Perez-Hormaeche J, Quintero FJ, Shin G, Kim MR, Qiang Z, Ning L, Park HC, Lee SY, Bressan RA, Pardo JM, Bohnert HJ, Yun DJ (2013) Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat Commun 4:1352CrossRefPubMedGoogle Scholar
  34. Krakauer DC, Nowak MA (1999) Evolutionary preservation of redundant duplicated genes. Semin Cell Develop Biol 10:555–559CrossRefGoogle Scholar
  35. Lindner H, Müller LM, Boisson-Dernier A, Grossniklaus U (2012) CrRLK1L receptor-like kinases: not just another brick in the wall. Curr Opin Plant Biol 6:659–669CrossRefGoogle Scholar
  36. McClung CR (2006) Plant circadian rhythms. Plant Cell 18:792–803CrossRefPubMedCentralPubMedGoogle Scholar
  37. Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19:1327–1331CrossRefPubMedGoogle Scholar
  38. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  39. Ngo QA, Vogler H, Lituiev DS, Nestorova A, Grossniklaus U (2014) A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Develop Cell 29:491–500CrossRefGoogle Scholar
  40. Nguyen MX, Moon S, Jung KH (2013) Genome-wide expression analysis of rice aquaporin genes and development of a functional gene network mediated by aquaporin expression in roots. Planta 238:669–681CrossRefPubMedGoogle Scholar
  41. Ogiso E, Takahashi Y, Sasaki T, Yano M, Izawa T (2010) The role of casein kinase II in flowering time regulation has diversified during evolution. Plant Physiol 152:808–820CrossRefPubMedCentralPubMedGoogle Scholar
  42. Oono Y, Yazawa T, Kawahara Y, Kanamori H, Kobayashi F, Sasaki H, Mori S, Wu J, Handa H, Itoh T (2014) Genome-wide transcriptome analysis reveals that cadmium stress signaling controls the expression of genes in drought stress signal pathways in rice. PLoS One 9:e96946CrossRefPubMedCentralPubMedGoogle Scholar
  43. Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure J-E (2003) Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 13:432–436CrossRefPubMedGoogle Scholar
  44. Schulze-Muth P, Irmler S, Schröder G, Schröder J (1996) Novel type of receptor-like protein kinase from a higher plant (Catharanthus roseus). cDNA, gene, intramolecular autophosphorylation, and identification of a threonine important for auto- and substrate phosphorylation. J Biol Chem 271:26684–26689CrossRefPubMedGoogle Scholar
  45. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227CrossRefPubMedGoogle Scholar
  46. Shiu S-H, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 2001:re22PubMedGoogle Scholar
  47. Sugiyama N, Izawa T, Oikawa T, Shimamoto K (2001) Light regulation of circadian clock-controlled gene expression in rice. Plant J 26:607–615CrossRefPubMedGoogle Scholar
  48. Wong ML, Medrano JF (2005) Real-time PCR for mRNA quantitation. Biotechniques 39:75CrossRefPubMedGoogle Scholar
  49. Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor App Gene 115:35–46CrossRefGoogle Scholar
  50. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2483CrossRefPubMedCentralPubMedGoogle Scholar
  51. Yu F, Qian L, Nibau C, Duan Q, Kita D, Levasseur K, Li X, Lu C, Li H, Hou C (2012) FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc Nat Acad Sci USA 109:14693–14698CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Quynh-Nga Nguyen
    • 1
  • Yang-Seok Lee
    • 1
  • Lae-Hyeon Cho
    • 1
  • Hee-Jeong Jeong
    • 1
  • Gynheung An
    • 1
    • 2
  • Ki-Hong Jung
    • 1
    • 2
  1. 1.Department of Plant Molecular Systems Biotechnology and Crop Biotech InstituteKyung Hee UniversityYonginKorea
  2. 2.Graduate School of BiotechnologyKyung Hee UniversityYonginKorea

Personalised recommendations