Abstract
We have previously proposed that Exo70A1 is required in the Brassicaceae stigma to control the early stages of pollen hydration and pollen tube penetration through the stigmatic surface, following compatible pollination. However, recent work has raised questions regarding Arabidopsis thaliana Exo70A1’s expression in the stigma and its role in stigma receptivity to compatible pollen. Here, we verified the expression of Exo70A1 in stigmas from three Brassicaceae species and carefully re-examined Exo70A1’s function in the stigmatic papillae. With previous studies showing that high relative humidity can rescue some pollination defects, essentially bypassing the control of pollen hydration by the Brassicaceae dry stigma, the effect of high humidity was investigated on pollinations with the Arabidopsis exo70A1-1 mutant. Pollinations under low relative humidity resulted in a complete failure of wild-type compatible pollen acceptance by the exo70A1-1 mutant stigma as we had previously seen. However, high relative humidity resulted in a partial rescue of the exo70A1-1 stigmatic papillar defect resulting is some wild-type compatible pollen acceptance and seed set. Thus, these results reaffirmed Exo70A1’s proposed role in the stigma regulating compatible pollen hydration and pollen tube entry and demonstrate that high relative humidity can partially bypass these functions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen AM, Thorogood CJ, Hegarty MJ, Lexer C, Hiscock SJ (2011) Pollen–pistil interactions and self-incompatibility in the Asteraceae: new insights from studies of Senecio squalidus (Oxford ragwort). Ann Bot 108(4):687–698
Chapman LA, Goring DR (2010) Pollen–pistil interactions regulating successful fertilization in the Brassicaceae. J Exp Bot 61(7):1987–1999
Chong YT, Gidda SK, Sanford C, Parkinson J, Mullen RT, Goring DR (2010) Characterization of the Arabidopsis thaliana exocyst complex gene families by phylogenetic, expression profiling, and subcellular localization studies. New Phytol 185(2):401–419
Dickinson H (1995) Dry stigmas, water and self-incompatibility in Brassica. Sex Plant Reprod 8(1):1–10
Drdova EJ, Synek L, Pecenkova T, Hala M, Kulich I, Fowler JE, Murphy AS, Zarsky V (2013) The exocyst complex contributes to PIN auxin efflux carrier recycling and polar auxin transport in Arabidopsis. Plant J 73(5):709–719
Fendrych M, Synek L, Pecenkova T, Toupalova H, Cole R, Drdova E, Nebesarova J, Sedinova M, Hala M, Fowler JE, Zarsky V (2010) The Arabidopsis exocyst complex is involved in cytokinesis and cell plate maturation. Plant Cell 22(9):3053–3065
Fendrych M, Synek L, Pecenkova T, Drdova EJ, Sekeres J, de Rycke R, Nowack MK, Zarsky V (2013) Visualization of the exocyst complex dynamics at the plasma membrane of Arabidopsis thaliana. Mol Biol Cell 24(4):510–520
Fiebig A, Mayfield JA, Miley NL, Chau S, Fischer RL, Preuss D (2000) Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12(10):2001–2008
Firon N, Nepi M, Pacini E (2012) Water status and associated processes mark critical stages in pollen development and functioning. Ann Bot 109(7):1201–1214
Fobis-Loisy I, Chambrier P, Gaude T (2007) Genetic transformation of Arabidopsis lyrata: specific expression of the green fluorescent protein (GFP) in pistil tissues. Plant Cell Rep 26(6):745–753
Foster E, Levesque-Lemay M, Schneiderman D, Albani D, Schernthaner J, Routly E, Robert LS (2005) Characterization of a gene highly expressed in the Brassica napus pistil that encodes a novel proline-rich protein. Sex Plant Reprod 17(6):261–267
Franklin TM, Oldknow J, Trick M (1996) SLR1 function is dispensable for both self-incompatible rejection and self-compatible pollination processes in Brassica. Sex Plant Reprod 9(4):203–208
Heider MR, Munson M (2012) Exorcising the exocyst complex. Traffic 13(7):898–907
Heslop-Harrison Y, Shivanna KR (1977) The receptive surface of the angiosperm stigma. Ann Bot 41:1233–1258
Hiscock SJ, Allen AM (2008) Diverse cell signalling pathways regulate pollen–stigma interactions: the search for consensus. New Phytol 179(2):286–317
Hulskamp M, Kopczak SD, Horejsi TF, Kihl BK, Pruitt RE (1995) Identification of genes required for pollen-stigma recognition in Arabidopsis thaliana. Plant J 8(5):703–714
Indriolo E, Tharmapalan P, Wright SI, Goring DR (2012) The ARC1 E3 ligase gene is frequently deleted in self-compatible Brassicaceae species and has a conserved role in Arabidopsis lyrata self-pollen rejection. Plant Cell 24(11):4607–4620
Indriolo E, Safavian D, Goring DR (2014) The ARC1 E3 ligase promotes two different self-pollen avoidance traits in Arabidopsis. Plant Cell 26(4):1525–1543
Johnson SA, McCormick S (2001) Pollen germinates precociously in the anthers of raring-to-go, an Arabidopsis gametophytic mutant. Plant Physiol 126(2):685–695
Kulich I, Cole R, Drdova E, Cvrckova F, Soukup A, Fowler J, Zarsky V (2010) Arabidopsis exocyst subunits SEC8 and EXO70A1 and exocyst interactor ROH1 are involved in the localized deposition of seed coat pectin. New Phytol 188(2):615–625
Li S, van Os GM, Ren S, Yu D, Ketelaar T, Emons AM, Liu CM (2010) Expression and functional analyses of EXO70 genes in Arabidopsis implicate their roles in regulating cell type-specific exocytosis. Plant Physiol 154(4):1819–1830
Li S, Chen M, Yu D, Ren S, Sun S, Liu L, Ketelaar T, Emons AM, Liu CM (2013) EXO70A1-mediated vesicle trafficking is critical for tracheary element development in Arabidopsis. Plant Cell 25(5):1774–1786
Pecenkova T, Hala M, Kulich I, Kocourkova D, Drdova E, Fendrych M, Toupalova H, Zarsky V (2011) The role for the exocyst complex subunits Exo70B2 and Exo70H1 in the plant-pathogen interaction. J Exp Bot 62(6):2107–2116
Preuss D, Lemieux B, Yen G, Davis RW (1993) A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes Dev 7(6):974–985
Safavian D, Goring DR (2013) Secretory activity is rapidly induced in stigmatic papillae by compatible pollen, but inhibited for self-incompatible pollen in the brassicaceae. PLoS ONE 8(12):e84286
Samuel MA, Chong YT, Haasen KE, Aldea-Brydges MG, Stone SL, Goring DR (2009) Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 21(9):2655–2671
Sanchez AM, Bosch M, Bots M, Nieuwland J, Feron R, Mariani C (2004) Pistil factors controlling pollination. Plant Cell 16:S98–S106
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767
Stegmann M, Anderson RG, Ichimura K, Pecenkova T, Reuter P, Zarsky V, McDowell JM, Shirasu K, Trujillo M (2012) The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis. Plant Cell 24(11):4703–4716
Swanson R, Edlund AF, Preuss D (2004) Species specificity in pollen-pistil interactions. Annu Rev Genet 38:793–818. doi:10.1146/annurev.genet.38.072902.092356
Synek L, Schlager N, Elias M, Quentin M, Hauser MT, Zarsky V (2006) AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J 48(1):54–72
Wang J, Ding Y, Hillmer S, Miao Y, Lo SW, Wang X, Robinson DG, Jiang L (2010) EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells. Plant Cell 22(12):4009–4030
Wang Y, Chu YJ, Xue HW (2012) Inositol polyphosphate 5-phosphatase-controlled Ins (1,4,5)P3/Ca2 + is crucial for maintaining pollen dormancy and regulating early germination of pollen. Development 139(12):2221–2233
Zárský V, Kulich I, Fendrych M, Pečenková T (2013) Exocyst complexes multiple functions in plant cells secretory pathways. Curr Opin Plant Biol 16(6):726–733
Acknowledgments
DS was supported by an Ontario Graduate Scholarship (OGS). This research was supported by grants from the Natural Sciences and Engineering Research Council of Canada to MAS and DRG, University start-up grants to MAS, and a Canada Research Chair to DRG.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by Zhenbiao Yang.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Safavian, D., Jamshed, M., Sankaranarayanan, S. et al. High humidity partially rescues the Arabidopsis thaliana exo70A1 stigmatic defect for accepting compatible pollen. Plant Reprod 27, 121–127 (2014). https://doi.org/10.1007/s00497-014-0245-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00497-014-0245-z