Integration of semi-in vivo assays and multi-omics data reveals the effect of galloylated catechins on self-pollen tube inhibition in Camellia oleifera

Yihong Chang , Wenfang Gong , Jinming Xu , Han Gong , Qiling Song , Shixin Xiao , Deyi Yuan

Horticulture Research ›› 2023, Vol. 10 ›› Issue (1) : 248

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (1) :248 DOI: 10.1093/hr/uhac248
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Integration of semi-in vivo assays and multi-omics data reveals the effect of galloylated catechins on self-pollen tube inhibition in Camellia oleifera
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Abstract

Camellia oil extracted from the seeds of Camellia oleifera Abel. is a popular and high-quality edible oil, but its yield is limited by seed setting, which is mainly caused by self-incompatibility (SI). One of the obvious biological features of SI plants is the inhibition of self-pollen tubes; however, the underlying mechanism of this inhibition in C. oleifera is poorly understood. In this study, we constructed a semi- in vivo pollen tube growth test (SIV-PGT) system that can screen for substances that inhibit self-pollen tubes without interference from the genetic background. Combined with multi-omics analysis, the results revealed the important role of galloylated catechins in self-pollen tube inhibition, and a possible molecular regulatory network mediated by UDP-glycosyltransferase ( UGT) and serine carboxypeptidase-like ( SCPL) was proposed. In summary, galloylation of catechins and high levels of galloylated catechins are specifically involved in pollen tube inhibition under self-pollination rather than cross-pollination, which provides a new understanding of SI in C. oleifera. These results will contribute to sexual reproduction research on C. oleifera and provide theoretical support for improving Camellia oil yield in production.

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Yihong Chang, Wenfang Gong, Jinming Xu, Han Gong, Qiling Song, Shixin Xiao, Deyi Yuan. Integration of semi-in vivo assays and multi-omics data reveals the effect of galloylated catechins on self-pollen tube inhibition in Camellia oleifera. Horticulture Research, 2023, 10 (1) : 248 DOI:10.1093/hr/uhac248

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Acknowledgement

Our work was supported by the National Key R&D Program of China (2018YFD1000603-1), the Natural Science Foundation of Hunan Province (2020JJ5968), Scientific Research Foundation for Advanced Talents of Central South University of Forestry and Technology (2018YJ002), Special Funds for the Construction of Innovative Provinces in Hunan (2021NK1007) and the Key Program of Education Department of Hunan Province (grant no. 20A524). We thank Dr. Yajun Liu for assistance with the galloylated catechin biosynthesis analysis.

Author contributions

Y.C., W.G., and D.Y. designed the experiment; Y.C., J.X., and H.G. carried out the experiment; Q.S. participated in the multi-omics data analysis; Y.C. wrote the manuscript; W.G. and S.X revised the manuscript. All authors read and approved the final manuscript.

Data availability

Metabolomics data have been deposited to the EMBL-EBI MetaboLights database with the identifier MTBLS5346. The mass spectrometry proteomics data have been deposited to the proteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD035406.

Conflict of interest

The authors declare that they have no conflicts of interest associated with this work.

Supplementary data

Supplementary data is available at Horticulture Research Journal online.

References

[1]

Vela P, Salinero C, Sainz MJ . Phenological growth stages of Camellia japonica . Ann Appl Biol. 2013; 162: 182-90.

[2]

Luan F, Zeng J, Yang Y et al. Recent advances in Camellia oleifera Abel: a review of nutritional constituents, biofunctional properties, and potential industrial applications . J Funct Foods. 2020; 75: 104242.

[3]

Takayama S, Isogai A . Self-incompatibility in plants. Annu Rev Plant Biol. 2005; 56: 467-89.

[4]

Jany E, Nelles H, Goring DR . The molecular and cellular regulation of Brassicaceae self-incompatibility and self-pollen rejection. Int. Rev. Cell Mol. Biol. 2019; 343: 1-35.

[5]

Nasrallah JB . Self-incompatibility in the Brassicaceae: Regulation and mechanism of self-recognition. Curr. Top. Dev. Biol. 2019; 131: 435-52.

[6]

Murase K, Shiba H, Iwano M et al. A membrane-anchored protein kinase involved in brassica self-incompatibility signaling. Science. 2004; 303: 1516-9.

[7]

Gu T, Mazzurco M, Sulaman W et al. Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase . Proc Natl Acad Sci U S A. 1998; 95: 382-7.

[8]

Samuel MA, Chong YT, Haasen KE et al. 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. 2009; 21: 2655-71.

[9]

Kao TH, Tsukamoto T . The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell. 2004; 16: S72-83.

[10]

Franklin-Tong N, Franklin FCH . Gametophytic self-incompatibility inhibits pollen tube growth using different mechanisms. Trends Plant Sci. 2003; 8: 598-605.

[11]

Liang M, Cao Z, Zhu A et al. Evolution of self-compatibility by a mutant S-m-RNase in citrus. Nat Plants. 2020; 6: 131-42.

[12]

Liu Z-Q, Xu G-H, Zhang S-L . Pyrus pyrifolia stylar S-RNase induces alterations in the actin cytoskeleton in self-pollen and tubes in vitro . Protoplasma. 2007; 232: 61-7.

[13]

Wang C-L, Wu J, Xu GH et al. S-RNase disrupts tip-localized reactive oxygen species and induces nuclear DNA degradation in incompatible pollen tubes of Pyrus pyrifolia . J Cell Sci. 2010; 123: 4301-9.

[14]

Franklin-Tong VE. Self-incompatibility in Papaver rhoeas: Progress in understanding mechanisms involved in regulating self-incompatibility in Papaver. In: Franklin-Tong VE, ed. Self-Incompatibility in Flowering Plants: Evolution, Diversity, and Mechanisms. Springer: Berlin Heidelberg, Berlin, Heidelberg, 2008, 237-58.

[15]

Wilkins KA, Poulter NS, Franklin-Tong VE . Taking one for the team: self-recognition and cell suicide in pollen. J Exp Bot 2014; 65: 1331-42.

[16]

Wang L, Lin Z, Triviño M et al. Self-incompatibility in Papaver pollen: programmed cell death in an acidic environment . J Exp Bot. 2019; 70: 2113-23.

[17]

Gao C, Yuan D, Ya Y et al. Anatomical characteristics of self-incompatibility in Camellia oleifera . Scientia Silvae Sinicae 2015; 51: 60-8.

[18]

Liao T, Yuan DY, Zou F et al. Self-sterility in Camellia oleifera may be due to the prezygotic late-acting self-incompatibility . PLoS One. 2014; 9: e99639.

[19]

Ma Q, Chen C, Zeng Z et al. Transcriptomic analysis between self- and cross-pollinated pistils of tea plants (Camellia sinensis) . BMC Genomics. 2018; 19: 289.

[20]

He Y, Song Q, Wu Y et al. TMT-based quantitative proteomic analysis reveals the crucial biological pathways involved in self-incompatibility responses in Camellia oleifera . Int J Mol Sci. 2020; 21: 1987.

[21]

Wang L, Lam PY, Lui ACW et al. Flavonoids are indispensable for complete male fertility in rice. J Exp Bot. 2020; 71: 4715-28.

[22]

Chen W, Xiao Z, Wang Y et al. Competition between anthocyanin and kaempferol glycosides biosynthesis affects pollen tube growth and seed set of malus . Hortic Res. 2021; 8: 173.

[23]

Yang Q, Song Z, Dong B et al. Hyperoside regulates its own biosynthesis via MYB30 in promoting reproductive development and seed set in okra. Plant Physiol. 2021; 185: 951-68.

[24]

Muhlemann Joëlle K, Younts Trenton LB et al. Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress. Proc Natl Acad Sci U S A. 2018; 115: E11188-97.

[25]

Jin JQ, Ma JQ, Ma CL et al. Determination of catechin content in representative chinese tea germplasms. J Agric Food Chem. 2014; 62: 9436-41.

[26]

Wei C, Yang H, Wang S et al. Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality . Proc Natl Acad Sci U S A. 2018; 115: E4151-8.

[27]

Gong W, Xiao S, Wang L et al. Chromosome-level genome of camellia lanceoleosa provides a valuable resource for understanding genome evolution and self-incompatibility . Plant J. 2022; 110: 881-98.

[28]

Higashiyama T, Kuroiwa H, Kawano S et al. Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri . Plant Cell. 1998; 10: 2019-31.

[29]

Takeuchi H, Higashiyama T . A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis . PLoS Biol. 2012; 10: e1001449.

[30]

Liu Y, Gao L, Liu L et al. Purification and characterization of a novel galloyltransferase involved in catechin galloylation in the tea plant (Camellia sinensis) . J Biol Chem. 2012; 287: 44406-17.

[31]

Yao S, Liu Y, Zhuang J et al. Insights into acylation mechanisms: co-expression of serine carboxypeptidase-like acyltransferases and their non-catalytic companion paralogs. Plant J. 2022; 111: 117-33.

[32]

Cui L, Yao S, Dai X et al. Identification of UDP-glycosyltransferases involved in the biosynthesis of astringent taste compounds in tea (Camellia sinensis) . J Exp Bot. 2016; 67: 2285-97.

[33]

Zhang CC, Wang LY, Wei K et al. Transcriptome analysis reveals self-incompatibility in the tea plant (Camellia sinensis) might be under gametophytic control . BMC Genomics. 2016; 17: 359.

[34]

Zhou J, Lu M, Yu S et al. In-depth understanding of Camellia oleifera self-incompatibility by comparative transcriptome, proteome and metabolome . Int J Mol Sci. 2020; 21: 1600.

[35]

He Y, Song Q, Chen S et al. Transcriptome analysis of self- and cross-pollinated pistils revealing candidate unigenes of self-incompatibility in Camellia oleifera . J Hortic Sci Biotechnol. 2020; 95: 19-31.

[36]

Okuda S, Tsutsui H, Shiina K et al. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature. 2009; 458: 357-61.

[37]

Duan Q, Liu MCJ, Kita D et al. FERONIA controls pectin- and nitric oxide-mediated male-female interaction. Nature. 2020; 579: 561-6.

[38]

Zhong S, Liu M, Wang Z et al. Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis . Science. 2019; 364: eaau9564.

[39]

Hafidh S, Potěšil D, Fíla J et al. Quantitative proteomics of the tobacco pollen tube secretome identifies novel pollen tube guidance proteins important for fertilization. Genome Biol. 2016; 17: 81.

[40]

Hafidh S, Honys D . Isolation of the pistil-stimulated pollen tube secretome. In: Geitmann A, ed. Pollen and Pollen Tube Biology: Methods and Protocols. Springer US: New York, NY, 2020, 41-72.

[41]

Lin SY, Chen PW, Chuang MH et al. Profiling of translatomes of in vivo-grown pollen tubes reveals genes with roles in micropylar guidance during pollination in Arabidopsis . Plant Cell. 2014; 26: 602-18.

[42]

Gu Z, Li W, Doughty J et al. A gamma-thionin protein from apple, MdD1, is required for defence against S-RNase-induced inhibition of pollen tube prior to self/non-self recognition. Plant Biotechnol J. 2019; 17: 2184-98.

[43]

Yang Q, Meng D, Gu Z et al. Apple S-RNase interacts with an actin-binding protein, MdMVG, to reduce pollen tube growth by inhibiting its actin-severing activity at the early stage of self-pollination induction. Plant J. 2018; 95: 41-56.

[44]

Li W, Meng D, Gu Z et al. Apple S-RNase triggers inhibition of tRNA aminoacylation by interacting with a soluble inorganic pyrophosphatase in growing self-pollen tubes in vitro . New Phytol. 2018; 218: 579-93.

[45]

Chen J, Wang P, de Graaf BHJ et al. Phosphatidic acid counteracts S-RNase signaling in pollen by stabilizing the actin cytoskeleton. Plant Cell. 2018; 30: 1023-39.

[46]

Wang CL, Xu GH, Jiang XT et al. S-RNase triggers mitochondrial alteration and DNA degradation in the incompatible pollen tube of Pyrus pyrifolia in vitro . Plant J. 2009; 57: 220-9.

[47]

Sato K, Nishio T, Kimura R et al. Coevolution of the S-locus genes SRK, SLG and SP11/SCR in Brassica oleracea and B. rapa . Genetics. 2002; 162: 931-40.

[48]

Kusaba M, Dwyer K, Hendershot J et al. Self-incompatibility in the genus Arabidopsis: characterization of the S locus in the outcrossing a. lyrata and its autogamous relative a. thaliana . Plant Cell. 2001; 13: 627-43.

[49]

Wu J, Gu C, Khan MA et al. Molecular determinants and mechanisms of gametophytic self-incompatibility in fruit trees of Rosaceae. Crit Rev Plant Sci. 2013; 32: 53-68.

[50]

Li K, Wang Y, Qu H . RNA-Seq analysis of compatible and incompatible styles of Pyrus species at the beginning of pollination . Plant Mol Biol. 2020; 102: 287-306.

[51]

Schopfer CR, Nasrallah ME, Nasrallah JB . The male determinant of self-incompatibility in brassica . Science. 1999; 286: 1697-700.

[52]

Takasaki T, Hatakeyama K, Suzuki G et al. The S receptor kinase determines self-incompatibility in Brassica stigma . Nature. 2000; 403: 913-6.

[53]

Takayama S, Shiba H, Iwano M et al. The pollen determinant of self-incompatibility in Brassica campestris . Proc Natl Acad Sci U S A. 2000; 97: 1920-5.

[54]

Anderson MA, Cornish EC, Mau SL et al. Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata . Nature. 1986; 321: 38-44.

[55]

Lai Z, Ma W, Han B et al. An F-box gene linked to the self-incompatibility (S) locus of antirrhinum is expressed specifically in pollen and tapetum . Plant Mol Biol. 2002; 50: 29-41.

[56]

Sassa H, Kakui H, Miyamoto M et al. S locus F-box brothers: multiple and pollen-specific F-box genes with S haplotype-specific polymorphisms in apple and Japanese pear . Genetics. 2007; 175: 1869-81.

[57]

Thomas SG, Franklin-Tong VE . Self-incompatibility triggers programmed cell death in Papaver pollen . Nature. 2004; 429: 305-9.

[58]

Wheeler MJ, de Graaf BHJ, Hadjiosif N et al. Identification of the pollen self-incompatibility determinant in Papaver rhoeas . Nature. 2009; 459: 992-5.

[59]

Shi D, Tang C, Wang R et al. Transcriptome and phytohormone analysis reveals a comprehensive phytohormone and pathogen defence response in pear self-/cross-pollination. Plant Cell Rep. 2017; 36: 1785-99.

[60]

Zhang L, Huang J, Su S et al. FERONIA receptor kinase-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa . Curr Biol. 2021; 31: 3004-3016.e4.

[61]

Chai L, Tudor RL, Poulter NS et al. MAP kinase PrMPK9-1 contributes to the self-incompatibility response. Plant Physiol. 2017; 174: 1226-37.

[62]

Lan X, Yang J, Abhinandan K et al. Flavonoids and ROS play opposing roles in mediating pollination in ornamental kale (Brassica oleracea var. acephala) . Mol Plant. 2017; 10: 1361-4.

[63]

Wang Y, Zhang WZ, Song LF et al. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis . Plant Physiol. 2008; 148: 1201-11.

[64]

Hoffmann RD, Portes MT, Olsen LI et al. Plasma membrane H +-ATPases sustain pollen tube growth and fertilization . Nat Commun. 2020; 11: 2395.

[65]

Alché JDD, Mrani-Alaoui M, Castro AJ, Rodríguez-García MI . Ole e 1, the major allergen from olive (Olea europaea L.) pollen, increases its expression and is released to the culture medium during in vitro germination . Plant Cell Physiol. 2004; 45: 1149-57.

[66]

Garabagi F, Duns G, Strommer J . Selective recruitment of Adh genes for distinct enzymatic functions in Petunia hybrida . Plant Mol Biol. 2005; 58: 283-94.

[67]

Hou Y, Guo X, Cyprys P et al. Maternal ENODLs are required for pollen tube reception in Arabidopsis . Curr Biol. 2016; 26: 2343-50.

[68]

Zhan H, Xiong H, Wang S et al. Anther endothecium-derived very-long-chain fatty acids facilitate pollen hydration in Arabidopsis . Mol Plant. 2018; 11: 1101-4.

[69]

Takahashi K, Shimada T, Kondo M et al. Ectopic expression of an esterase, which is a candidate for the unidentified plant cutinase, causes cuticular defects in Arabidopsis thaliana . Plant Cell Physiol. 2010; 51: 123-31.

[70]

Chen H-Y, Li X . Identification of a residue responsible for UDP-sugar donor selectivity of a dihydroxybenzoic acid glycosyltransferase from Arabidopsis natural accessions . Plant J. 2017; 89:195203.

[71]

Lindner H, Kessler SA, Müller LM et al. TURAN and EVAN mediate pollen tube reception in Arabidopsis synergids through protein glycosylation . PLoS Biol. 2015; 13: 1002139.

[72]

Muller LM, Lindner H, Pires ND et al. A subunit of the oligosaccharyltransferase complex is required for interspecific gametophyte recognition in Arabidopsis . Nat Commun. 2016; 7: 10826.

[73]

Hruba P, Honys D, Twell D et al. Expression of β-galactosidase and β-xylosidase genes during microspore and pollen development . Planta. 2005; 220: 931-40.

[74]

Chen W, Gong L, Guo Z et al. A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol Plant. 2013; 6: 1769-80.

[75]

Ahmad MZ, Li P, She G et al. Genome-wide analysis of serine carboxypeptidase-like acyltransferase gene family for evolution and characterization of enzymes involved in the biosynthesis of galloylated catechins in the tea plant (Camellia sinensis) . Front Plant Sci. 2020; 11: 848.

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