The maize ( Zea mays L.) roothairless3 gene encodes a putative GPI‐anchored, monocot‐specific, COBRA‐like protein that significantly affects grain yield

Abstract

Summary The rth3 ( roothairless 3 ) mutant is specifically affected in root hair elongation. We report here the cloning of the rth3 gene via a PCR‐based strategy (amplification of insertion mutagenized sites) and demonstrate that it encodes a COBRA‐like protein that displays all the structural features of a glycosylphosphatidylinositol anchor. Genes of the COBRA family are involved in various types of cell expansion and cell wall biosynthesis. The rth3 gene belongs to a monocot‐specific clade of the COBRA gene family comprising two maize and two rice genes. While the rice ( Oryza sativa ) gene OsBC1L1 appears to be orthologous to rth3 based on sequence similarity (86% identity at the protein level) and maize/rice synteny, the maize ( Zea mays L.) rth3‐like gene does not appear to be a functional homolog of rth3 based on their distinct expression profiles. Massively parallel signature sequencing analysis detected rth3 expression in all analyzed tissues, but at relatively low levels, with the most abundant expression in primary roots where the root hair phenotype is manifested. In situ hybridization experiments confine rth3 expression to root hair‐forming epidermal cells and lateral root primordia. Remarkably, in replicated field trials involving near‐isogenic lines, the rth3 mutant conferred significant losses in grain yield.

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References 50

1. 1.

   Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389-3402.

   Not in our library10.1093/nar/25.17.3389

2. 2.

   Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. Current Protocols in Molecular Biology. 1994.

   Not in our library

3. 3.

   Brady SM, Song S, Dhugga KS, Rafalski JA, Benfey PN. Combining expression and comparative evolutionary analysis. The COBRA gene family. Plant Physiol. 2007;143:172-187.

   Not in our library10.1104/pp.106.087262

4. 4.

   Brenner S, Johnson M, Bridgham J, et al. Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat. Biotechnol. 2000;18:630-634.

   Not in our library10.1038/76469

5. 5.

   Brown DM, Zeef LAH, Ellis J, Goodacre R, Turner SR. Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell. 2005;17:2281-2295.

   Not in our library10.1105/tpc.105.031542

6. 6.

   Burr B, Burr FA. Recombinant inbreds for molecular mapping in maize: theoretical and practical considerations. Trends Genet. 1991;7:55-60.

   Not in our library10.1016/0168-9525(91)90232-f

7. 7.

   Burr B, Burr FA, Thompson KH, Albertson MC, Stuber CW. Gene mapping with recombinant inbreds in maize. Genetics. 1988;118:519-526.

   Not in our library10.1093/genetics/118.3.519

8. 8.

   Carpita N, McCann M, Buchanan B, Gruissem W, Jones R. The cell wall. Biochemistry and Molecular Biology of Plants. 2000;52-109.

   Not in our library

9. 9.

   Ching A, Dhugga KS, Appenzeller L, Meeley R, Bourett TM, Howard RJ, Rafalski A. Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchored protein that affects mechanical strength of maize tissues by altering the composition and structure of secondary cell walls. Planta. 2006;224:1174-1184.

   Not in our library10.1007/s00425-006-0299-8

10. 10.

    Ciamporova M, Dekankova K, Hanackova Z, Peters P, Ovecka M, Baluska F. Structural aspects of bulge formation during root hair initiation. Plant and Soil. 2003;255:1-7.

    Not in our library

11. 11.

    Cobbett CS. Phytochelatines and their roles in heavy metal detoxification. Plant Physiol. 2000;123:825-832.

    Not in our library10.1104/pp.123.3.825

12. 12.

    Coe E, Freeling M, Walbot V. Genetic experiments and mapping. The Maize Handbook. 1994;189-197.

    Not in our library

13. 13.

    Cui X, Hsia A-P, Liu F, Ashlock DA, Wise RP, Schnable PS. Alternative transcription initiation sites and polyadenylation sites are recruited during Mu suppression at the rf2a locus of maize. Genetics. 2003;163:685-698.

    Not in our library10.1093/genetics/163.2.685

14. 14.

    Dolan L, Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K. Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development. 1994;120:2465-2474.

    Not in our library

15. 15.

    Eisenhaber B, Bork P, Eisenhaber F. Prediction of potential GPI-modification sites in proprotein sequences. J. Mol. Biol. 1999;292:741-758.

    Not in our library10.1006/jmbi.1999.3069

16. 16.

    Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003;422:442-446.

    Not in our library10.1038/nature01485

17. 17.

    Frey M, Stettner C, Gierl A. A general method for gene isolation in tagging approaches: amplification of insertion mutagenised sites (AIMS). Plant J. 1998;13:717-722.

    Not in our library

18. 18.

    Gale MD, Devos KM. Plant comparative genetics after 10 years. Science. 1998;282:656-659.

    Not in our library10.1126/science.282.5389.656

19. 19.

    Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A, Walker JM. Protein identification and analysis tools on the ExPASy server. The Proteomics Protocols Handbook. 2005;571-607.

    Not in our library

20. 20.

    Gilroy S, Jones DL. Through form to function: root hair development and nutrient uptake. Trends Plant Sci. 2000;5:56-60.

    Not in our library10.1016/s1360-1385(99)01551-4

21. 21.

    Gough J, Karplus K, Hughey R, Chothia C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J. Mol. Biol. 2001;313:903-919.

    Not in our library10.1006/jmbi.2001.5080

22. 22.

    Hochholdinger F, Park WJ, Sauer M, Woll K. From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci. 2004a;9:42-48.

    Not in our library10.1016/j.tplants.2003.11.003

23. 23.

    Hochholdinger F, Woll K, Sauer M, Dembinsky D. Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programs. Annals Bot. 2004b;93:359-368.

    Not in our library10.1093/aob/mch056

24. 24.

    Horton P, Park K-J, Obayashi T, Nakai K. Protein Subcellular Localization Prediction with WoLFPSORT. 2006;39-48.

    Not in our library

25. 25.

    Jackson D, Gurr SR, McPherson MJ, Bowles DJ. In situ hybridization in plants. Molecular Plant Pathology: A Practical Approach. 1992;163-174.

    Not in our library

26. 26.

    Jones MA, Raymond MJ, Smirnoff N. Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J. 2006;45:83-100.

    Not in our library10.1111/j.1365-313x.2005.02609.x

27. 27.

    Kropf DL, Bisgrove SR, Hable WE. Differing roles of the cytoskeleton in intercalary growth and tip growth of plant cells. Curr. Opin. Cell Biol. 1998;10:117-122.

    Not in our library10.1016/s0955-0674(98)80094-x

28. 28.

    Kyte J, Doolittle R. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982;157:105-132.

    Not in our library10.1016/0022-2836(82)90515-0

29. 29.

    Larkin JC, Brown ML, Schiefelbein J. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu. Rev. Plant. Biol. 2003;54:403-430.

    Not in our library10.1146/annurev.arplant.54.031902.134823

30. 30.

    Lee MM, Schiefelbein J. Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell. 2002;14:611-618.

    Not in our library10.1105/tpc.010434

31. 31.

    Leuchter R, Wolf K, Zimmermann M. Isolation of an Arabidopsis cDNA complementing a Schizosaccharomyces pombe mutant deficient in phytochelatin synthesis. Plant Physiol. 1998;117:331-333.

    Not in our library

32. 32.
    A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium · 1997

    Not checked
33. 33.

    Li Y, Qian Q, Zhou Y, et al. BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell. 2003;15:2020-2031.

    Not in our library10.1105/tpc.011775

34. 34.

    Morgan BA, Conlon FL, Manzanares M, Millar JBA, Kanuga N, Sharpe J, Krumlauf R, Smith JC, Sedgwick SG. Transposon tools for recombination DNA manipulation: characterization of transcriptional regulators from yeast, Xenopus, and mouse. Proc. Natl Acad. Sci. USA. 1996;93:2801-2806.

    Not in our library10.1073/pnas.93.7.2801

35. 35.

    Parker JS, Cavell AC, Dolan L, Robert K, Grierson CS. Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell. 2000;12:1961-1974.

    Not in our library10.1105/tpc.12.10.1961

36. 36.

    Persson S, Wei H, Milne J, Page GP, Somerville CR. Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc. Natl Acad. Sci. USA. 2005;102:8633-8638.

    Not in our library10.1073/pnas.0503392102

37. 37.

    Rigas S, Debrosses G, Haralampidis K, Vicente-Aqullo F, Feldman KA. TRP1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell. 2001;13:139-151.

    Not in our library10.1105/tpc.13.1.139

38. 38.

    Roudier F, Schindelman G, DeSalle R, Benfey PN. The COBRA family of putative GPI-anchored proteins in Arabidopsis. A new fellowship in expansion. Plant Physiol. 2002;130:538-548.

    Not in our library10.1104/pp.007468

39. 39.

    Roudier F, Fernandez AG, Fujita M, et al. COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell. 2005;17:1749-1763.

    Not in our library10.1105/tpc.105.031732

40. 40.

    Row HC, Reeder JR. Root-hair development as evidence of relationships among genera of gramineae. Am. J. Bot. 1957;44:596-601.

    Not in our library

41. 41.

    Schindelman G, Morikami A, Jungm J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN. COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev. 2001;15:1115-1127.

    Not in our library10.1101/gad.879101

42. 42.

    Sieberer B, Emons AMC. Cytoarchitecture and pattern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors. Protoplasma. 2000;214:118-127.

    Not in our library

43. 43.

    Stinard PS, Robertson DS, Schnable PS. Genetic isolation, cloning, and analysis of a Mutator-induced, dominant antimorph of the maize amylose extender1 locus. Plant Cell. 1993;5:1555-1566.

    Not in our library10.1105/tpc.5.11.1555

44. 44.

    Taramino G, Sauer M, Stauffer J, Multani D, Niu X, Sakai H, Hochholdinger F. The rtcs gene in maize (Zea mays L.) encodes a lob domain protein that is required for postembryonic shoot-borne and embryonic seminal root initiation. Plant J. 2007;50:649-659.

    Not in our library10.1111/j.1365-313x.2007.03075.x

45. 45.

    Udenfriend S, Kodukula K. How glycosyl-phosphatidylinositol-anchored membrane-proteins are made. Annu. Rev. Biochem. 1995;64:563-591.

    Not in our library10.1146/annurev.bi.64.070195.003023

46. 46.

    Wang H, Lockwood SK, Hoeltzel MF, Schiefelbein JW. The ROOT HAIR DEFECTIVE3 gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required fro regulated cell enlargement in Arabidopsis. Genes Dev. 1997;11:799-811.

    Not in our library10.1101/gad.11.6.799

47. 47.

    Wasteneys GO, Galway ME. Remodeling the cytoskeleton for growth and form: an overview with some new views. Annu. Rev. Plant. Biol. 2003;54:691-722.

    Not in our library10.1146/annurev.arplant.54.031902.134818

48. 48.

    Wen TJ, Schnable PS. Analyses of mutants of three genes that influence root hair development in Zea mays (Gramineae) suggest that root hairs are dispensable. Am. J. Bot. 1994;81:833-842.

    Not in our library

49. 49.

    Wen TJ, Hochholdinger F, Sauer M, Bruce W, Schnable PS. The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol. 2005;138:1637-1643.

    Not in our library10.1104/pp.105.062174

50. 50.

    Zimmermann R, Werr W. Pattern formation in the monocot embryo as revealed by NAM and CUC3 orthologues from Zea mays L. Plant Mol. Biol. 2005;58:669-685.

    Not in our library10.1007/s11103-005-7702-x

Cited by papers we hold 2

• Genome-wide association analysis of seedling root development in maize (Zea mays L.) · 2015
  No notice
• Brittle Culm1, a COBRA-Like Protein, Functions in Cellulose Assembly through Binding Cellulose Microfibrils · 2013
  No notice

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