Rapid identification of a natural knockout allele of armadillo repeat-containing kinesin1 that causes root hair branching by mapping-by-sequencing

Plant Physiology

Volumn 166, Issue 3, 2014, Pages 1280-1287

  Rishmawi, Louai ^a   Sun, Hequan ^b   Schneeberger, Korbinian ^b   Hülskamp, Martin ^a   Schrader, Andrea ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; ARMADILLO DOMAIN PROTEIN; KINESIN; MRH2 PROTEIN, ARABIDOPSIS;

ALLELE; ANIMAL; ARABIDOPSIS; ARMADILLO; CHROMOSOME MAP; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; PLANT ROOT; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARMADILLO DOMAIN PROTEINS; ARMADILLOS; CHROMOSOME MAPPING; KINESIN; MUTATION; PHENOTYPE; PLANT ROOTS; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84908565338     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.244046     Document Type: Article

References (55)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
2. Autran D, Baroux C, Raissig MT, Lenormand T, Wittig M, Grob S, Steimer A, Barann M, Klostermeier UC, Leblanc O, et al (2011) Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145: 707-719
3. Baluska F, Salaj J, Mathur J, Braun M, Jasper F, Samaj J, Chua NH, Barlow PW, Volkmann D (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227: 618-632
4. Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17: 657-665
5. Brunak S, Engelbrecht J, Knudsen S (1991) Prediction of human mRNA donor and acceptor sites from the DNA sequence. J Mol Biol 220: 49-65
6. Cantor RM, Lange K, Sinsheimer JS (2010) Prioritizing GWAS results: a review of statistical methods and recommendations for their application. Am J Hum Genet 86: 6-22
7. Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, Fitz J, Koenig D, Lanz C, Stegle O, Lippert C, et al (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43: 956-963
8. Carol RJ, Dolan L (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci 357: 815-821
9. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438: 1013-1016
10. Charif D, Lobry J (2007) SeqinR 1.0-2: a contributed package to the R Project for Statistical Computing devoted to biological sequences retrieval and analysis. In U Bastolla, M Porto, HE Roman, M Vendruscolo, eds, Structural Approaches to Sequence Evolution. Springer, Berlin, Heidelberg, pp 207-232
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
12. Drouaud J, Camilleri C, Bourguignon PY, Canaguier A, Bérard A, Vezon D, Giancola S, Brunel D, Colot V, Prum B, et al (2006) Variation in crossingover rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination “hot spots”. Genome Res 16: 106-114
13. Drouaud J, Mercier R, Chelysheva L, Bérard A, Falque M, Martin O, Zanni V, Brunel D, Mézard C (2007) Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet 3: e106
14. Eng RC, Wasteneys GO (2014) The microtubule plus-end tracking protein ARMADILLO-REPEAT KINESIN1 promotes microtubule catastrophe in Arabidopsis. Plant Cell 26: 3372-3386
15. Era A, Tominaga M, Ebine K, Awai C, Saito C, Ishizaki K, Yamato KT, Kohchi T, Nakano A, Ueda T (2009) Application of Lifeact reveals F-actin dynamics in Arabidopsis thaliana and the liverwort, Marchantia polymorpha. Plant Cell Physiol 50: 1041-1048
16. Failmezger H, Jaegle B, Schrader A, Hülskamp M, Tresch A (2013) Semiautomated 3D leaf reconstruction and analysis of trichome patterning from light microscopic images. PLoS Comput Biol 9: e1003029
17. Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C, Cabral A, Parker JE (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17: 2601-2613
18. Fitz Gerald JN, Carlson AL, Smith E, Maloof JN, Weigel D, Chory J, Borevitz JO, Swanson RJ (2014) New Arabidopsis advanced intercross recombinant inbred lines reveal female control of nonrandom mating. Plant Physiol 165: 175-185
19. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446
20. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, et al (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419-423
21. Hartwig B, James GV, Konrad K, Schneeberger K, Turck F (2012) Fast isogenic mapping-by-sequencing of ethyl methanesulfonate-induced mutant bulks. Plant Physiol 160: 591-600
22. Hebsgaard SM, Korning PG, Tolstrup N, Engelbrecht J, Rouzé P, Brunak S (1996) Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res 24: 3439-3452
23. Heilmann I (2009) Using genetic tools to understand plant phosphoinositide signalling. Trends Plant Sci 14: 171-179
24. James GV, Patel V, Nordström KJ, Klasen JR, Salomé PA, Weigel D, Schneeberger K (2013) User guide for mapping-by-sequencing in Arabidopsis. Genome Biol 14: R61
25. Jombart T (2008) adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403-1405
26. Jones MA, Raymond MJ, Smirnoff N (2006) Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 45: 83-100
27. Jones MA, Shen JJ, Fu Y, Li H, Yang Z, Grierson CS (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14: 763-776
28. Kim S, Plagnol V, Hu TT, Toomajian C, Clark RM, Ossowski S, Ecker JR, Weigel D, Nordborg M (2007) Recombination and linkage disequilibrium in Arabidopsis thaliana. Nat Genet 39: 1151-1155
29. Kirik V, Schrader A, Uhrig JF, Hulskamp M (2007) MIDGET unravels functions of the Arabidopsis topoisomerase VI complex in DNA endoreduplication, chromatin condensation, and transcriptional silencing. Plant Cell 19: 3100-3110
30. Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9: 29
31. Lee YJ, Yang Z (2008) Tip growth: signaling in the apical dome. Curr Opin Plant Biol 11: 662-671
32. Long Q, Rabanal FA, Meng D, Huber CD, Farlow A, Platzer A, Zhang Q, Vilhjálmsson BJ, Korte A, Nizhynska V, et al (2013) Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat Genet 45: 884-890
33. Miller DD, De Ruijter NCA, Bisseling T, Emons AmC (1999) The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J 17: 141-154
34. Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K (2001) Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J 20: 2779-2788
35. Müller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134: 409-419
36. Nordström KJ, Albani MC, James GV, Gutjahr C, Hartwig B, Turck F, Paszkowski U, Coupland G, Schneeberger K (2013) Mutation identification by direct comparison of whole-genome sequencing data from mutant and wild-type individuals using k-mers. Nat Biotechnol 31: 325-330
37. Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D (2008) Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res 18: 2024-2033
38. Payne RJ, Grierson CS (2009) A theoretical model for ROP localisation by auxin in Arabidopsis root hair cells. PLoS ONE 4: e8337
39. Preuss ML, Kovar DR, Lee YR, Staiger CJ, Delmer DP, Liu B (2004) A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol 136: 3945-3955
40. Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172: 991-998
41. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna
42. Rishmawi L, Pesch M, Juengst C, Schauss AC, Schrader A, Hülskamp M (2014) Non-cell-autonomous regulation of root hair patterning genes by WRKY75 in Arabidopsis. Plant Physiol 165: 186-195
43. Sakai T, Honing Hv, Nishioka M, Uehara Y, Takahashi M, Fujisawa N, Saji K, Seki M, Shinozaki K, Jones MA, et al (2008) Armadillo repeatcontaining kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis. Plant J 53: 157-171
44. Salomé PA, Bomblies K, Fitz J, Laitinen RA, Warthmann N, Yant L, Weigel D (2012) The recombination landscape in Arabidopsis thaliana F2 populations. Heredity (Edinb) 108: 447-455
45. Samaj J, Baluska F, Voigt B, Schlicht M, Volkmann D, Menzel D (2004) Endocytosis, actin cytoskeleton, and signaling. Plant Physiol 135: 1150-1161
46. Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, Alix A, McCosh RB, Chen H, Schork NJ, et al (2013) Patterns of population epigenomic diversity. Nature 495: 193-198
47. Schneeberger K, Hagmann J, Ossowski S, Warthmann N, Gesing S, Kohlbacher O, Weigel D (2009a) Simultaneous alignment of short reads against multiple genomes. Genome Biol 10: R98
48. Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, Jørgensen JE, Weigel D, Andersen SU (2009b) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods 6: 550-551
49. Shimada TL, Shimada T, Hara-Nishimura I (2010) A rapid and nondestructive screenable marker, FAST, for identifying transformed seeds of Arabidopsis thaliana. Plant J 61: 519-528
50. Steffens A, Jaegle B, Tresch A, Hülskamp M, Jakoby M (2014) Processingbody movement in Arabidopsis depends on an interaction between myosins and DECAPPING PROTEIN1. Plant Physiol 164: 1879-1892
51. Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, et al (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74: 174-183
52. Thole JM, Vermeer JE, Zhang Y, Gadella TW Jr, Nielsen E (2008) Root hair defective4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20: 381-395
53. Yang G, Gao P, Zhang H, Huang S, Zheng ZL (2007) A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 small GTPase in Arabidopsis. PLoS ONE 2: e1074
54. Yoo CM, Blancaflor EB (2013) Overlapping and divergent signaling pathways for ARK1 and AGD1 in the control of root hair polarity in Arabidopsis thaliana. Front Plant Sci 4: 528
55. Yoo CM, Wen J, Motes CM, Sparks JA, Blancaflor EB (2008) A class I ADPribosylation factor GTPase-activating protein is critical for maintaining directional root hair growth in Arabidopsis. Plant Physiol 147: 1659-1674