Skip to main content
Genetics logoLink to Genetics
. 2004 Jul;167(3):1381–1394. doi: 10.1534/genetics.104.026575

Clonal mosaic analysis of EMPTY PERICARP2 reveals nonredundant functions of the duplicated HEAT SHOCK FACTOR BINDING PROTEINs during maize shoot development.

Suneng Fu 1, Michael J Scanlon 1
PMCID: PMC1470956  PMID: 15280250

Abstract

The paralogous maize proteins EMPTY PERICARP2 (EMP2) and HEAT SHOCK FACTOR BINDING PROTEIN2 (HSBP2) each contain a single recognizable motif: the coiled-coil domain. EMP2 and HSBP2 accumulate differentially during maize development and heat stress. Previous analyses revealed that EMP2 is required for regulation of heat shock protein (hsp) gene expression and also for embryo morphogenesis. Developmentally abnormal emp2 mutant embryos are aborted during early embryogenesis. To analyze EMP2 function during postembryonic stages, plants mosaic for sectors of emp2 mutant tissue were constructed. Clonal sectors of emp2 mutant tissue revealed multiple defects during maize vegetative shoot development, but these sector phenotypes are not correlated with aberrant hsp gene regulation. Furthermore, equivalent phenotypes are observed in emp2 sectored plants grown under heat stress and nonstress conditions. Thus, the function of EMP2 during regulation of the heat stress response can be separated from its role in plant development. The discovery of emp2 mutant phenotypes in postembryonic shoots reveals that the duplicate genes emp2 and hsbp2 encode nonredundant functions throughout maize development. Distinct developmental phenotypes correlated with the developmental timing, position, and tissue layer of emp2 mutant sectors, suggesting that EMP2 has evolved diverse developmental functions in the maize shoot.

Full Text

The Full Text of this article is available as a PDF (553.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Becraft P. W., Bongard-Pierce D. K., Sylvester A. W., Poethig R. S., Freeling M. The liguleless-1 gene acts tissue specifically in maize leaf development. Dev Biol. 1990 Sep;141(1):220–232. doi: 10.1016/0012-1606(90)90117-2. [DOI] [PubMed] [Google Scholar]
  2. Becraft P. W., Freeling M. Sectors of liguleless-1 tissue interrupt an inductive signal during maize leaf development. Plant Cell. 1991 Aug;3(8):801–807. doi: 10.1105/tpc.3.8.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burkhard P., Stetefeld J., Strelkov S. V. Coiled coils: a highly versatile protein folding motif. Trends Cell Biol. 2001 Feb;11(2):82–88. doi: 10.1016/s0962-8924(00)01898-5. [DOI] [PubMed] [Google Scholar]
  4. Foster T., Veit B., Hake S. Mosaic analysis of the dominant mutant, Gnarley1-R, reveals distinct lateral and transverse signaling pathways during maize leaf development. Development. 1999 Jan;126(2):305–313. doi: 10.1242/dev.126.2.305. [DOI] [PubMed] [Google Scholar]
  5. Fu Suneng, Meeley Robert, Scanlon Michael J. Empty pericarp2 encodes a negative regulator of the heat shock response and is required for maize embryogenesis. Plant Cell. 2002 Dec;14(12):3119–3132. doi: 10.1105/tpc.006726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gurley W. B., Key J. L. Transcriptional regulation of the heat-shock response: a plant perspective. Biochemistry. 1991 Jan 8;30(1):1–12. doi: 10.1021/bi00215a001. [DOI] [PubMed] [Google Scholar]
  7. Harper L., Freeling M. Interactions of liguleless1 and liguleless2 function during ligule induction in maize. Genetics. 1996 Dec;144(4):1871–1882. doi: 10.1093/genetics/144.4.1871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Lindquist S. The heat-shock response. Annu Rev Biochem. 1986;55:1151–1191. doi: 10.1146/annurev.bi.55.070186.005443. [DOI] [PubMed] [Google Scholar]
  9. Lund A. A., Blum P. H., Bhattramakki D., Elthon T. E. Heat-stress response of maize mitochondria. Plant Physiol. 1998 Mar;116(3):1097–1110. doi: 10.1104/pp.116.3.1097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Marrs K. A., Casey E. S., Capitant S. A., Bouchard R. A., Dietrich P. S., Mettler I. J., Sinibaldi R. M. Characterization of two maize HSP90 heat shock protein genes: expression during heat shock, embryogenesis, and pollen development. Dev Genet. 1993;14(1):27–41. doi: 10.1002/dvg.1020140105. [DOI] [PubMed] [Google Scholar]
  11. Mitchell H. K., Lipps L. S. Heat shock and phenocopy induction in Drosophila. Cell. 1978 Nov;15(3):907–918. doi: 10.1016/0092-8674(78)90275-1. [DOI] [PubMed] [Google Scholar]
  12. Morimoto R. I. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 1998 Dec 15;12(24):3788–3796. doi: 10.1101/gad.12.24.3788. [DOI] [PubMed] [Google Scholar]
  13. Nardmann Judith, Ji Jiabing, Werr Wolfgang, Scanlon Michael J. The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development. 2004 Jun;131(12):2827–2839. doi: 10.1242/dev.01164. [DOI] [PubMed] [Google Scholar]
  14. Newman John R. S., Keating Amy E. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science. 2003 Jun 12;300(5628):2097–2101. doi: 10.1126/science.1084648. [DOI] [PubMed] [Google Scholar]
  15. Nieto-Sotelo Jorge, Martínez Luz María, Ponce Georgina, Cassab Gladys I., Alagón Alejandro, Meeley Robert B., Ribaut Jean-Marcel, Yang Runying. Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. Plant Cell. 2002 Jul;14(7):1621–1633. doi: 10.1105/tpc.010487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Petersen N. S., Mitchell H. K. The induction of a multiple wing hair phenocopy by heat shock in mutant heterozygotes. Dev Biol. 1987 Jun;121(2):335–341. doi: 10.1016/0012-1606(87)90169-2. [DOI] [PubMed] [Google Scholar]
  17. Pirkkala L., Nykänen P., Sistonen L. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 2001 May;15(7):1118–1131. doi: 10.1096/fj00-0294rev. [DOI] [PubMed] [Google Scholar]
  18. Queitsch Christine, Sangster Todd A., Lindquist Susan. Hsp90 as a capacitor of phenotypic variation. Nature. 2002 May 12;417(6889):618–624. doi: 10.1038/nature749. [DOI] [PubMed] [Google Scholar]
  19. Reinhardt D., Mandel T., Kuhlemeier C. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell. 2000 Apr;12(4):507–518. doi: 10.1105/tpc.12.4.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Reinhardt D., Wittwer F., Mandel T., Kuhlemeier C. Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell. 1998 Sep;10(9):1427–1437. doi: 10.1105/tpc.10.9.1427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Reinhardt Didier, Pesce Eva-Rachele, Stieger Pia, Mandel Therese, Baltensperger Kurt, Bennett Malcolm, Traas Jan, Friml Jirí, Kuhlemeier Cris. Regulation of phyllotaxis by polar auxin transport. Nature. 2003 Nov 20;426(6964):255–260. doi: 10.1038/nature02081. [DOI] [PubMed] [Google Scholar]
  22. Satyal S. H., Chen D., Fox S. G., Kramer J. M., Morimoto R. I. Negative regulation of the heat shock transcriptional response by HSBP1. Genes Dev. 1998 Jul 1;12(13):1962–1974. doi: 10.1101/gad.12.13.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Scanlon M. J., Freeling M. Clonal sectors reveal that a specific meristematic domain is not utilized in the maize mutant narrow sheath. Dev Biol. 1997 Feb 1;182(1):52–66. doi: 10.1006/dbio.1996.8452. [DOI] [PubMed] [Google Scholar]
  24. Scanlon M. J. NARROW SHEATH1 functions from two meristematic foci during founder-cell recruitment in maize leaf development. Development. 2000 Nov;127(21):4573–4585. doi: 10.1242/dev.127.21.4573. [DOI] [PubMed] [Google Scholar]
  25. Sylvester A. W., Cande W. Z., Freeling M. Division and differentiation during normal and liguleless-1 maize leaf development. Development. 1990 Nov;110(3):985–1000. doi: 10.1242/dev.110.3.985. [DOI] [PubMed] [Google Scholar]
  26. Tai Li-Jung, McFall Sally M., Huang Kai, Demeler Borries, Fox Sue G., Brubaker Kurt, Radhakrishnan Ishwar, Morimoto Richard I. Structure-function analysis of the heat shock factor-binding protein reveals a protein composed solely of a highly conserved and dynamic coiled-coil trimerization domain. J Biol Chem. 2001 Oct 25;277(1):735–745. doi: 10.1074/jbc.M108604200. [DOI] [PubMed] [Google Scholar]
  27. Veit B., Briggs S. P., Schmidt R. J., Yanofsky M. F., Hake S. Regulation of leaf initiation by the terminal ear 1 gene of maize. Nature. 1998 May 14;393(6681):166–168. doi: 10.1038/30239. [DOI] [PubMed] [Google Scholar]
  28. Vernoux T., Kronenberger J., Grandjean O., Laufs P., Traas J. PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development. 2000 Dec;127(23):5157–5165. doi: 10.1242/dev.127.23.5157. [DOI] [PubMed] [Google Scholar]
  29. Vierling E., Harris L. M., Chen Q. The major low-molecular-weight heat shock protein in chloroplasts shows antigenic conservation among diverse higher plant species. Mol Cell Biol. 1989 Feb;9(2):461–468. doi: 10.1128/mcb.9.2.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wiederrecht G., Seto D., Parker C. S. Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell. 1988 Sep 9;54(6):841–853. doi: 10.1016/s0092-8674(88)91197-x. [DOI] [PubMed] [Google Scholar]
  31. Young T. E., Ling J., Geisler-Lee C. J., Tanguay R. L., Caldwell C., Gallie D. R. Developmental and thermal regulation of the maize heat shock protein, HSP101. Plant Physiol. 2001 Nov;127(3):777–791. [PMC free article] [PubMed] [Google Scholar]
  32. Yu Y. Bruce. Coiled-coils: stability, specificity, and drug delivery potential. Adv Drug Deliv Rev. 2002 Oct 18;54(8):1113–1129. doi: 10.1016/s0169-409x(02)00058-3. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES