Abstract
Heteromorphic self-incompatibility (HetSI) is a strategy used to prevent selfing while favouring outcrossing in angiosperm. Although the genome, proteome and metabolome of homomorphic self-incompatibility (HomSI) have been investigated, metabolome findings have shown that energy deficiency is one of the factors leading to HomSI. However, the mechanism of HetSI remains unclear. This study investigates the alterations of metabolite fluxes in HetSI. Here, metabolic changes present in dimorphic styles as well as between self-incompatibility (SI) and self-compatibility (SC) pollinations of Plumbago auriculata Lam were simultaneously determined by gas chromatography–mass spectrometry (GC–MS). Fifty-three metabolites, mainly including other organic acids, amino acids, carbohydrates/glycosides, fatty acids/lipids, amines, amides, flavonoids and alcohols, were detected. The overall results showed that carbohydrates, which may affect pollen germination and pollen tube growth rate on stigmas, were abundant in S (short styles without pollination). Moreover, energy deficiency may not be a reason for HetSI because we found inflated levels of metabolites in SI pollinations. This study provided detailed insight into metabolic changes in HetSI and evidence for further studies of HetSI.
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References
Baker HG (1953a) Dimorphism and monomorphism in the Plumbaginaceae. II. Pollen and stigmata in the genus Limonium. Ann Bot 17:433–445. https://doi.org/10.1093/oxfordjournals.aob.a083361
Baker HG (1953b) Dimorphism and monomorphism in the Plumbaginaceae. III. Correlation of geographical distribution patterns with dimorphism and monomorphism in Limonium. Ann Bot 17:615–628. https://doi.org/10.1093/oxfordjournals.aob.a083374
Dulberger R (1975) Intermorph structural differences between stigmatic papillae and pollen grains in relation to incompatibility in Plumbaginaceae. P R Soc Lond B Biol 188:257–274. https://doi.org/10.1098/rspb.1975.0018
Fernie AR (2007) The future of metabolic phytochemistry: larger numbers of metabolites, higher resolution, greater understanding. Phytochemistry 68:2861–2880. https://doi.org/10.1016/j.phytochem.2007.07.010
Fiehn O (2002) Metabolomics—the link between genotypes and phenotypes. Plant Mol Biol 48:155–171. https://doi.org/10.1007/978-94-010-0448-0_11
Fragallah SADA, Wang P, Li N, Chen Y, Lin S (2018) Metabolomic analysis of pollen grains with different germination abilities from two clones of Chinese fir (Cunninghamia lanceolata (Lamb) Hook). Molecules 23:3162. https://doi.org/10.3390/molecules23123162
Franklin-Tong N, Franklin FCH (2003) Gametophytic self-incompatibility inhibits pollen tube growth using different mechanisms. Trends Plant Sci 8:598–605. https://doi.org/10.1016/j.tplants.2003.10.008
Goetz M, Guivarćh A, Hirsche J, Bauerfeind MA, González M-C, Hyun TK, Eom SH, Chriqui D, Engelke T, Großkinsky DK, Roitsch T (2017) Metabolic control of tobacco pollination by sugars and invertases. Plant Physiol 173:984–997. https://doi.org/10.1104/pp.16.01601
Heizmann P, Luu DT, Dumas C (2000) Pollen–stigma adhesion in the brassicaceae. Ann Bot 85:23–27. https://doi.org/10.1006/anbo.1999.1057
Hu D, Li W, Gao S, Lei T, Hu J, Shen P, Li Y, Li J (2019) Untargeted metabolomic profiling reveals that different responses to self and cross pollination in each flower morph of the heteromorphic plant Plumbago auriculata. Plant Physiol Biochem 144:413–426. https://doi.org/10.1016/j.plaphy.2019.10.010
Ischebeck T (2016) Lipids in pollen—they are different. Biochim Biophys Acta 1861:1315–1328. https://doi.org/10.1016/j.bbalip.2016.03.023
Kim HK, Choi YH, Verpoorte R (2011) NMR-based plant metabolomics: where do we stand, where do we go? Trends Biotechnol 29:267–275. https://doi.org/10.1016/j.tibtech.2011.02.001
Kitasiba H, Nishio T (2013) Self-incompatibility. Biotechnol Crucif 2:187–208. https://doi.org/10.1007/978-1-4614-7795-2_10
Lloyd DG, Webb CJ (1992) The evolution of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 151–178
Loewus F, Labarca C (1973) Pistil-secretion product and pollen tube wall formation. In: Loewus F (ed) Biogenesis of plant cell wall polysacharrides. Academic Press, New York, pp 175–193
Mandrone M, Antognoni F, Aloisi I, Potente G, Poli F, Cai G, Faleri C, Parrotta L, Del Duca S (2019) Compatible and incompatible pollen-styles interaction in Pyrus communis L. show different transglutaminase features, polyamine pattern and metabolomics profiles. Front Plant Sci 10:741. https://doi.org/10.3389/fpls.2019.00741
Mo Y, Nagel C, Taylor LP (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc Natl Acad Sci USA 89:7213–7217. https://doi.org/10.1073/pnas.89.15.7213
Parrotta L, Faleri C, Del Duca S, Cai G (2018) Depletion of sucrose induces changes in the tip growth mechanism of tobacco pollen tubes. Ann Bot Lond 122:23–43. https://doi.org/10.1093/aob/mcy043
Swarcewicz B, Sawikowska A, Marczak L, Luczak M, Ciesiołka D, Krystkowiak K, Kuczyńska A, Piślewska-Bednarek M, Krajewski P, Stobiecki M (2017) Effect of drought stress on metabolite contents in barley recombinant inbred line population revealed by untargeted GC–MS profiling. Acta Physiol Plant 39:158. https://doi.org/10.1007/s11738-017-2449-y
Wang G-M, Gu C, Qiao X, Zhao B-Y, Ke Y-Q, Guo B-B, Hao P-P, Qi K-J, Zhang S-L (2017) Characteristic of pollen tube that grew into self style in pear cultivar and parent assignment for cross-pollination. Sci Hortic 216:226–233. https://doi.org/10.1016/j.scienta.2016.10.035
Yue X, Gao X-Q, Wang F, Dong Y, Li X, Zhang XS (2014) transcriptional evidence for inferred pattern of pollen tube-stigma metabolic coupling during pollination. PLoS ONE 9:e107046. https://doi.org/10.1371/journal.pone.0107046
Zeng J, Gao Q, Shi S, Lian X, Converse R, Zhang H, Yang X, Ren X, Chen S, Zhu L (2017) Dissecting pistil responses to incompatible and compatible pollen in self-incompatibility Brassica oleracea using comparative proteomics. Protein J 36:123–137. https://doi.org/10.1007/s10930-017-9697-y
Zhao P, Pan Q, Yu W, Zhao L (2016) Dissect style response to pollination using metabolite profiling in self-compatible and self-incompatible tomato species. J Chromatogr B 1017–1018:153–162. https://doi.org/10.1016/j.jchromb.2016.01.056
Acknowledgements
This work was supported by the National Key R&D Program of China (2018YFD0600105) and the Sichuan Science and Technology Program (2018JY0211).
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Hu, D., Gao, S., Li, W. et al. Dissecting the distyly response to pollination using metabolite profiling in heteromorphic incompatibility system interactions of Plumbago auriculata Lam. Acta Physiol Plant 42, 122 (2020). https://doi.org/10.1007/s11738-020-03111-2
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DOI: https://doi.org/10.1007/s11738-020-03111-2