Skip to main content
SpringerLink
Log in

Effect of sporophytic PIRL9 genotype on post-meiotic expression of the Arabidopsis pirl1;pirl9 mutant pollen phenotype

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Plant intracellular ras-group-related leucine-rich repeat proteins (PIRLs) are a novel class of plant leucine-rich repeat (LRR) proteins structurally related to animal ras-group LRRs involved in cell signaling and gene regulation. Gene knockout analysis has shown that two members of the Arabidopsis thaliana PIRL gene family, PIRL1 and PIRL9, are redundant and essential for pollen development and viability: pirl1;pirl9 microspores produced by pirl1/PIRL1;pirl9 plants consistently abort just before pollen mitosis I. qrt1 tetrad analysis demonstrated that the genes become essential after meiosis, during anther stage 10. In this study, we characterized the phenotype of pirl1;pirl9 pollen produced by plants heterozygous for pirl9 (pirl1;pirl9/PIRL9). Alexander’s staining, scanning electron microscopy, and fluorescence microscopy indicated that pirl1;pirl9 double mutants produced by pirl9 heterozygotes have a less severe phenotype and more variable morphology than pirl1;pirl9 pollen from pirl1/PIRL1;pirl9 plants. Mutant pollen underwent developmental arrest with variable timing, often progressing beyond pollen mitosis I and arresting at the binucleate stage. Thus, although the pirl1 and pirl9 mutations act post-meiosis, the timing and expressivity of the pirl1;pirl9 pollen phenotype depends on the pirl9 genotype of the parent plant. These results suggest a continued requirement for PIRL1 and PIRL9 beyond the initiation of pollen mitosis. Furthermore, they reveal a modest but novel sporophytic effect in which parent plant genotype influences a mutant phenotype expressed in the haploid generation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

DAPI:

4′,6-Diamidino-2-phenylindole

LRR:

Leucine-rich repeat

PIRL:

Plant intracellular ras-group-related LRR protein

SEM:

Scanning electron microscopy

References

  • Alexander MP (1969) Differential staining of aborted and non-aborted pollen. Stain Technol 41:117–122

    Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Baez JM, Riveros M, Lehnback C (2002) Viability and longevity of pollen of Nothofagus species in south Chile. N Z J Bot 40:671–678

    Article  Google Scholar 

  • Belkhadir Y, Subramaniam R, Dangl JL (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 7:391–399

    Article  CAS  PubMed  Google Scholar 

  • Bouche N, Bouchez D (2001) Arabidopsis gene knockout: phenotypes wanted. Curr Opin Plant Biol 4:111–117

    Article  CAS  PubMed  Google Scholar 

  • Briggs GC, Osmont KS, Shindo C, Sibout R, Hardtke CS (2006) Unequal genetic redundancies in Arabidopsis—a neglected phenomenon? Trends Plant Sci 11:492–498

    Article  CAS  PubMed  Google Scholar 

  • Buchanan SG, Gay NJ (1996) Structural and functional diversity in the leucine-rich repeat family of proteins. Prog Biophys Mol Biol 65:1–44

    Article  CAS  PubMed  Google Scholar 

  • Claudianos C, Campbell HD (1995) The novel flightless-I gene brings together two gene families, actin-binding proteins related to gelsolin and leucine-rich-repeat proteins involved in Ras signal transduction. Mol Biol Evol 12:405–414

    CAS  PubMed  Google Scholar 

  • Cushing DA, Forsthoefel NR, Gestaut DR, Vernon DM (2005) Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221:424–436

    Article  CAS  PubMed  Google Scholar 

  • Cutler ML, Bassin RH, Zanoni L, Talbot N (1992) Isolation of rsp-1, a novel cDNA capable of suppressing v-Ras transformation. Mol Cell Biol 12:3750–3756

    CAS  PubMed  Google Scholar 

  • Dafini A, Devan P, Husband B (2005) Practical pollination biology. Enviroquest Ltd, Canada, p 590

    Google Scholar 

  • Dai P, Xiong WC, Mei L (2006) Erbin inhibits RAF activation by disrupting the sur-8-Ras-Raf complex. J Biol Chem 281:927–933

    Article  CAS  PubMed  Google Scholar 

  • De Smet I, Voss U, Jurgens G, Beeckman T (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173

    Article  PubMed  Google Scholar 

  • Dievart A, Clark SE (2004) LRR-containing receptors regulating plant development and defense. Development 131:251–261

    Article  CAS  PubMed  Google Scholar 

  • Dougherty GW, Jose C, Gimona M, Cutler ML (2008) The Rsu-1-PINCH1-ILK complex is regulated by Ras activation in tumor cells. Eur J Cell Biol 87:721–734

    Article  CAS  PubMed  Google Scholar 

  • Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13(4):472–477

    Article  CAS  PubMed  Google Scholar 

  • Fluhr R (2001) Sentinels of disease. Plant resistance genes. Plant Physiol 127:1367–1374

    Article  CAS  PubMed  Google Scholar 

  • Forsthoefel NR, Cutler K, Port MD, Yamamoto T, Vernon DM (2005) PIRLs: a novel class of plant intracellular leucine-rich repeat proteins. Plant Cell Physiol 46:913–922

    Article  CAS  PubMed  Google Scholar 

  • Forsthoefel NR, Dao TP, Vernon DM (2010) PIRL1 and PIRL9, encoding members of a novel plant-specific family of leucine-rich repeat proteins, are essential for differentiation of microspores into pollen. Planta 232(5):1101–1114

    Google Scholar 

  • Hellmann H, Estelle M (2002) Plant development: regulation by protein degradation. Science 297:793–797

    Article  CAS  PubMed  Google Scholar 

  • Jeong KW, Lee YH, Stallcup MR (2009) Recruitment of the SWI/SNF chromatin remodeling complex to steroid hormone-regulated promoters by nuclear receptor coactivator flightless-I. J Biol Chem 284:29298–29309

    Article  CAS  PubMed  Google Scholar 

  • Johnson-Brousseau SA, McCormick S (2004) A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant J 39:761–775

    Article  CAS  PubMed  Google Scholar 

  • Lee YH, Campbell HD, Stallcup MR (2004) Developmentally essential protein flightless I is a nuclear receptor coactivator with actin binding activity. Mol Cell Biol 24:2103–2117

    Article  CAS  PubMed  Google Scholar 

  • Li W, Han M, Guan KL (2000) The leucine-rich repeat protein SUR-8 enhances MAP kinase activation and forms a complex with Ras and Raf. Genes Dev 14:895–900

    CAS  PubMed  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

    Article  PubMed  Google Scholar 

  • Morillo SA, Tax FE (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opin Plant Biol 9:460–469

    Article  CAS  PubMed  Google Scholar 

  • Morris ER, Walker JC (2003) Receptor-like protein kinases: the keys to response. Curr Opin Plant Biol 6:339–342

    Article  CAS  PubMed  Google Scholar 

  • Preuss D, Rhee SY, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264:1458–1460

    Article  CAS  PubMed  Google Scholar 

  • Sieburth DS, Sun Q, Han M (1998) SUR-8, a conserved Ras-binding protein with leucine-rich repeats, positively regulates Ras-mediated signaling in C. elegans. Cell 94:119–130

    Article  CAS  PubMed  Google Scholar 

  • Somers DE, Fujiwara S (2009) Thinking outside the F-box: novel ligands for novel receptors. Trends Plant Sci 14:206–213

    Article  CAS  PubMed  Google Scholar 

  • Sternberg PW, Alberola-Ila J (1998) Conspiracy theory: RAS and RAF do not act alone. Cell 95:447–450

    Article  CAS  PubMed  Google Scholar 

  • Tax FE, Vernon DM (2001) T-DNA-associated duplication/translocations in Arabidopsis. Implications for mutant analysis and functional genomics. Plant Physiol 126:1527–1538

    Article  CAS  PubMed  Google Scholar 

  • Vernon DM, Forsthoefel NR (2002) Leucine-rich repeat proteins in plants: diverse roles in signaling and development. In: Pandali SG (ed) Research signpost: recent research developments in plant biology, pp 202–214

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV et al (2007) An electronic fluorescent pictograph browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2(8):e718

    Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by NSF award 0616166 to D.M.V. Whitman College’s SEM facility was provided by NSF grant 0922978. We thank Thuy Dao for assistance with PCR and phenotype analyses, and Michelle Shafer and Caroline Reinhart for assistance with SEM. Caroline Reinhart was supported in part by a Voyles summer research scholarship, provided by a gift to Whitman College.

Author information

Authors and Affiliations

  1. Department of Biology, Whitman College, Walla Walla, WA, 99362, USA

    Nancy R. Forsthoefel & Daniel M. Vernon

  2. Program in Biochemistry, Biophysics and Molecular Biology, Whitman College, 345 Boyer Avenue, Walla Walla, WA, 99362, USA

    Daniel M. Vernon

Authors
  1. Nancy R. Forsthoefel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel M. Vernon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel M. Vernon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forsthoefel, N.R., Vernon, D.M. Effect of sporophytic PIRL9 genotype on post-meiotic expression of the Arabidopsis pirl1;pirl9 mutant pollen phenotype. Planta 233, 423–431 (2011). https://doi.org/10.1007/s00425-010-1324-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1324-5

Keywords

Search

Navigation