Abstract
Nicotiana alata is a model species used to study gametophytic self-incompatibility (SI), controlled by the S-locus (encoding S-RNase and SLF proteins expressed in pistil and pollen, respectively) as well as by modifier genes (such as 120 kDa, HT-b and Trxh). A previous study revealed that SI in N. alata accession S2S2 was plastic, and that SI was leaky with senescence of the pistil and plant. Here, we further explored its regulatory mechanisms. Reverse transcription quantitative PCR (RT-qPCR) and western blot results showed that during the senescence of pistil in S2S2, 120 kDa and HT-b were transcribed and translated at lower levels, while marked residual S-RNase activity was detected. The transcripts of Trxh varied irregularly. Only the transcription and translation of 120 kDa declined with the plant senescence. According to the results, PSF in S2S2 may be associated with down-regulated expression of 120 kDa and HT-b, while S-RNase and Trxh seem to be unrelated to this phenotype. These findings deepen our understanding of the regulatory mechanisms of SI plasticity in N. alata.
Similar content being viewed by others
References
Ai YJ, Kron E, Kao TH (1991) S-alleles are retained and expressed in a self-compatible cultivar of Petunia hybrida. Mol Gen Genet 230:353–358
Akagi T, Henry IM, Morimoto T, Tao R (2016) Insights into the Prunus-specific S-RNase-based self-incompatibility system from a genome-wide analysis of the evolutionary radiation of S locus-related F-box genes. Plant Cell Physiol 57:1281–1294
Ascher PD, Peloquin S (1966) Effect of floral aging on the growth of compatible and incompatible pollen tubes in Lilium longiflorum. Am J Bot 53:99–102
Ávila-Castañeda A, Juárez-Díaz JA, Rodríguez-Sotres R et al (2014) A novel motif in the NaTrxh N-terminus promotes its secretion, whereas the C-terminus participates in its interaction with S-RNase in vitro. BMC Plant Biol 14:1–16
Brown PH, Ho THD (1986) Barley Aleurone Layers Secrete a Nuclease in Response to Gibberellic Acid: Purification and Partial Characterization of the Associated Ribonuclease, Deoxyribonuclease, and 3′-Nucleotidase Activities. Plant Physiol 82:801–806
Cruz-Garcia F, Hancock CN, Kim D et al (2005) Stylar glycoproteins bind to S-RNase in vitro. Plant J 42:295–304
Dodds PN, Bönig I, Du H et al (1993) S-RNase gene of Nicotiana alata is expressed in developing pollen. Plant Cell 5:1771–1782
Fan P, Wang X, Kuang T et al (2009) An efficient method for the extraction of chloroplast proteins compatible for 2-DE and MS analysis. Electrophoresis 30:3024–3033
Franklin-Tong VE (2008) Self-incompatibility in flowering plants. Springer, Berlin, vol 5, pp 640–645
Garcia-Valencia LE, Bravo-Alberto CE, Wu HM et al (2017) SIPP, a novel mitochondrial phosphate carrier mediates in self-incompatibility. Plant Physiol 175:1105–1120
Goldraij A, Kondo K, Lee CB et al (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439:805–810
Good-Avila SV, Stephenson AG (2002) The inheritance of modifiers conferring self-fertility in the partially self-incompatibilty perennial, Campanula rapunculoides L. (Campanulaceae). Evolution 56: 263–272
Good-Avila SV, Mena-Alı´ JI, Stephenson AG (2008) Genetic and environmental causes and evolutionary consequences of variations in self-fertility in self incompatible species. Springer, Berlin, pp 33–51
Hancock CN, Kent L, Mcclure BA (2005) The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43:716–723
Huang J, Zhao L, Yang QY et al (2006) AhSSK1, a novel SKP1-like protein that interacts with the S-locus F-box protein SLF. Plant J 46:780–793
Iwano M, Takayama S (2012) Self/non-self discrimination in angiosperm self-incompatibility. Curr Opin Plant Biol 15:78–83
Jahnen W, Batterham MP, Clarke AE et al (1989) Identification, isolation, and N-terminal sequencing of style glycoproteins associated with self-incompatibility in Nicotiana alata. Plant Cell 1:493–499
Juárezdíaz JA, Mcclure B, Vázquezsantana S et al (2006) A novel thioredoxin h is secreted in Nicotiana alata and reduces S-RNase in vitro. J BiolChem 281:3418–3424
Kaufmann H, Kirch H, Wemmer T et al (1992) Sporophytic and gametophytic self-incompatibility. Springer, Berlin, pp 115–125
Kondo K, Yamamoto M, Matton DP et al (2002) Cultivated tomato has defects in both S-RNase and HT genes required for stylar function of self-incompatibility. Plant J 29:627–636
Lai Z, Ma W, Han B et al (2002) An F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol 50:29–42
Levin DA (1996) The evolutionary significance of pseudo-self-fertility. Am Nat 148:321–332
Liao JG, Dai JR, Kang HM et al (2016) Plasticity in the self-incompatibility system of cultivated Nicotiana alata. Euphytica 208:129–141
Lind JL, Bönig I, Clarke AE et al (1996) A style-specific 120 kDa glycoprotein enters pollen tubes of Nicotiana alata in vivo. Sex Plant Reprod 9:75–86
Liu W, Fan JB, Li JH et al (2014) SCF(SLF)-mediated cytosolic degradation of S-RNase is required for cross-pollen compatibility in S-RNase-based self-incompatibility in Petunia hybrida. Front Genet 5:228
Lloyd DG (1992) Self-and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci 153:370–380
McClure B (2004) S-RNase and SLF determine S-haplotype-specific pollen recognition and rejection. Plant Cell 16:2840–2847
McClure B (2006) New views of S-RNase-based self-incompatibility. Curr Opin Plant Biol 9:639–646
McClure B, Cruz-Garcia F, Romero C (2011) Compatibility and incompatibility in S-RNase-based systems. Ann Bot 108:647–658
McClure B, Mou B, Canevascini S et al (1999) A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Nati A Sci 96:13548–13553
McClure BA, Franklin-Tong V (2006) Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition. Planta 224:233–245
Meng X, Sun P, Kao TH (2011) S-RNase-based self-incompatibility in Petunia inflata. Ann Bot 108:637–646
O’Brien M, Kapfer C, Major G et al (2002) Molecular analysis of the stylar-expressed Solanum chacoense small asparagine-rich protein family related to the HT modifier of gametophytic self-incompatibility in Nicotiana. Plant J 32:985–996
Pandey KK (1960) Evolution of gametophytic and sporophytic systems of self-incomaptibility in angiosperms. Evolution 14:98–115
Puerta AR, Ushijima K, Koba T et al (2009) Identification and functional analysis of pistil self-incompatibility factor HT-B of Petunia. J Exp Bot 60:1309
Qi X, Luu DT, Yang Q et al (2001) Genotype-dependent differences in S12-RNase expression lead to sporadic self-compatibility. Plant Mol Biol 45:295–305
Qin XK, Liu B, Soulard J et al (2006) Style-by-style analysis of two sporadic self-compatible Solanum chacoense lines supports a primary role for S-RNases in determining pollen rejection thresholds. J Exp Bot 57(9):2001–2013
Qiao H, Wang H, Zhao L et al (2004) The F-box protein AhSLF-S2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S proteasome pathway of protein degradation during compatible pollination in Antirrhinum. Plant Cell 16:582–595
Skirpan AL, Mccubbin AG, Sijacic P et al (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305
Steinbachs JE, Holsinger KE (2002) S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Mol Biol Evol 19:825–829
Takayama S, Isogai A (2005) Self-incompatibility in plants. Ann Rev Plant Biol 56:467–489
Tovar-Mendez A, Lu L, McClure B (2017) HT proteins contribute to S-RNase-independent pollen rejection in Solanum. Plant J 89:718–729
Tsukamoto T, Ando T, Takahashi K et al (2003) Breakdown of self-incompatibility in a natural population of Petunia axillaris caused by loss of pollen function. Plant Physiol 131:1903–1912
Vieira J, Fonseca NA, Vieira CP (2008) An S-RNase-based gametophytic self-Incompatibility system evolved only once in eudicots. J Mol Evolution 67:179–190
Williams JS, Wu L, Li S et al (2015) Insight into S-RNase-based self-incompatibility in Petunia: recent findings and future directions. Front Plant Sci 6:41
Zhao L, Ding Q, Zeng J et al (2012) An improved CTAB- ammonium acetate method for total RNA isolation from cotton. Phytochem Analysis 23(6):647–650
Acknowledgements
We are very grateful to Professor Xuejun Chen (Yunnan Academy of Tobacco Agricultural Sciences) for providing the seeds and genotype of the N.alata material. This study was supported by Grants 31560419 and 31660067 from the National Natural Science Fund in China, Grants 2017KY05 and 2018530000241034 from Yuxi Zhongyan Tobacco Seed Co., Ltd..
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Liao, J., Wei, X., Chen, Z. et al. Research on the regulatory mechanisms of self-incompatibility plasticity in Nicotiana alata. Euphytica 216, 149 (2020). https://doi.org/10.1007/s10681-020-02687-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-020-02687-7