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RNA-Seq analysis of compatible and incompatible styles of Pyrus species at the beginning of pollination

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At the early stage of pollination, the difference in gene expression between compatibility and incompatibility is highly significant about the pollen-specific expression of the LRR gene, resistance, and defensin genes.

Abstract

In Rosaceae, incompatible pollen can penetrate into the style during the gametophytic self-incompatibility response. It is therefore considered a stylar event rather than a stigmatic event. In this study, we explored the differences in gene expression between compatibility and incompatibility in the early stage of pollination. The self-compatible pear variety “Jinzhuili” is a naturally occurring bud mutant from “Yali”, a leading Chinese native cultivar exhibiting typical gametophytic self-incompatibility. We collected the styles of ‘Yali’ and ‘Jinzhuili’ at 0.5 and 2 h after self-pollination and then performed high-throughput sequencing. According to the KEGG analysis of the differentially expressed genes, several metabolic pathways, such as “Plant hormone signal transduction”, “Plant-pathogen interaction”, are the main pathways was the most represented pathway. Quantitative PCR was used to validate these differential genes. The expression levels of genes related to pollen growth and disease inhibition, such as LRR (Leucine-rich repeat extensin), resistance, defensin, and auxin, differed significantly between compatible and incompatible pollination. Interestingly, at 0.5 h, most of these genes were upregulated in the compatible pollination system compared with the incompatible pollination system. Calcium transport, which requires ATPase, also demonstrated upregulated expression. In summary, the self-incompatibility reaction was initiated when the pollen land on the stigma.

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References

  • Austin AT, Ballaré CL (2014) Plant interactions with other organisms: molecules, ecology and evolution. New Phytol 204:257–260

    Article  PubMed  Google Scholar 

  • Chae K, Lord EM (2011) Pollen tube growth and guidance: roles of small, secreted proteins. Ann Bot 108:627–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Wang P, de Graaf BHJ, Zhang H, Jiao H, Tang C, Zhang S, Wu J (2018a) Phosphatidic acid counteracts s-rnase signaling in pollen by stabilizing the actin cytoskeleton. Plant Cell 30:1023–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Wang P, de Graaf BHJ, Zhang H, Jiao H, Tang C, Zhang S, Wu J (2018b) Phosphatidic acid counteracts S-RNase signaling in pollen by stabilizing the actin cytoskeleton. Plant Cell 30(5):1023–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Claessen H, Keulemans W, Van de Poel B, De Storme N (2019) Finding a compatible partner: self-incompatibility in european pear (Pyrus communis); molecular control, genetic determination, and impact on fertilization and fruit set. Front Plant Sci 10:407

    Article  PubMed  PubMed Central  Google Scholar 

  • Covey PA, Subbaiah CC, Parsons RL, Pearce G, Lay FT, Anderson MA, Ryan CA, Bedinger PA (2010) A pollen-specific RALF from tomato that regulates pollen tube elongation. Plant Physiol 153:703–715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz-Garcia F, Hancock CN, McClure B (2003) S-RNase complexes and pollen rejection. J Exp Bot 54:123–130

    Article  CAS  PubMed  Google Scholar 

  • Doucet J, Lee HK, Goring DR (2016) Pollen acceptance or rejection: a tale of two pathways. Trends Plant Sci 21:1058–1067

    Article  CAS  PubMed  Google Scholar 

  • Draghici S, Khatri P, Tarca AL, Amin K, Done A, Voichita C, Georgescu C, Romero R (2007) A systems biology approach for pathway level analysis. Genome Res 17:1537–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dresselhaus T, Sprunck S, Wessel G (2016) Fertilization mechanisms in flowering plants. Curr Biol 26:R125–R139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii S, Tsuchimatsu T, Kimura Y, Ishida S, Tangpranomkorn S, Shimosato-Asano H, Iwano M, Furukawa S, Itoyama W, Wada Y, Shimizu KK, Takayama S (2019) A stigmatic gene confers interspecies incompatibility in the Brassicaceae. Nat Plants 5:731–741

    Article  CAS  PubMed  Google Scholar 

  • Gao Y, Liu H, Pei D (2014) Morphological characteristics and in situ auxin production during the histogenesis of staminate flowers in precocious walnut. J Am Soc Hotic Sci 139(2):185–190

    Article  CAS  Google Scholar 

  • Geitmann A, Franklintong VE, Emons AC (2004) The self-incompatibility response in Papaver rhoeas pollen causes early and striking alterations to organelles. Cell Death Differ 11:812–822

    Article  CAS  PubMed  Google Scholar 

  • Halász J, Hegedûs A (2006) Self-incompatibility in pears (Pyrus communis L., Pyrus serotina Rehd. and Pyrus ussuriensis) review. Int J Horticult Sci 12(2):87–91

    Google Scholar 

  • Hepler PK, Winship LJ (2015) The pollen tube clear zone: clues to the mechanism of polarized growth. J Integr Plant Biol 57:79–92

    Article  CAS  PubMed  Google Scholar 

  • Hill AE, ShacharHill B, Skepper JN, Powell J, ShacharHill Y (2012) An osmotic model of the growing pollen tube. PLoS ONE 7:e36585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiscock SJ, Mcinnis SM (2004) Pollen recognition and rejection during the sporophytic self-incompatibility response: Brassica and beyond. Trends Plant Sci 8:606–613

    Article  CAS  Google Scholar 

  • Hodgkin T, Lyon GD, Dickinson HG (1988) Recognition in flowering plants: a comparison of the Brassica self-incompatibility system and plant pathogen interactions. New Phytol 110:557–569

    Article  Google Scholar 

  • Igic B, Bohs L, Kohn JR (2004) Historical inferences from the self-incompatibility locus. New Phytol 161:97–105

    Article  CAS  Google Scholar 

  • Jones DA, Jdg J (1997) The role of leucine-rich repeat proteins in plant defences. Adv Bot Res 24:89–167

    Article  Google Scholar 

  • Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:277–280

    Article  CAS  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kovaleva L, Zakharova E (2003) Hormonal status of the pollen-pistil system at the progamic phase of fertilization after compatible and incompatible pollination in Petunia hybrida L. Sex Plant Reprod 16:191–196

    Article  CAS  Google Scholar 

  • Kovaleva LV, Zakharova EV, Skorobogatova IV, Karsunkina NP (2002) Gametophyte sporophyte Interactions in the Pollen Pistil System: 3. Hormonal Status at the Progamic Phase of Fertilization. Russ J Plant Physiol 49:492–495

    Article  CAS  Google Scholar 

  • Lamport DTA, Li T, Held MA, Kieliszewski MJ (2018) Pollen tube growth and guidance: Occam’s razor sharpened on a molecular arabinogalactan glycoprotein Rosetta Stone. New Phytol 217:491–500

    Article  CAS  PubMed  Google Scholar 

  • Liu Z-Q, Xu G-H, Zhang S-L (2007) Pyrus pyrifolia stylar S-RNase induces alterations in the actin cytoskeleton in self-pollen and tubes in vitro. Protoplasma 232:61–67

    Article  PubMed  Google Scholar 

  • Matsumoto D, Tao R (2016) Distinct self-recognition in the prunus S-RNase-based gametophytic self-incompatibility system. Hortic J 85:289–305

    Article  CAS  Google Scholar 

  • Matsumoto D, Tao R (2019) Recognition of S-RNases by an S locus F-box like protein and an S haplotype-specific F-box like protein in the Prunus-specific self-incompatibility system. Plant Mol Biol 100:367–378

    Article  CAS  PubMed  Google Scholar 

  • McClure B (2006) New views of S-RNase-based self-incompatibility. Curr Opin Plant Biol 9:639–646

    Article  CAS  PubMed  Google Scholar 

  • Mecchia MA, Santosfernandez G, Duss NN, Somoza SC, Boissondernier A, Gagliardini V, MartC-nezbernardini A, Fabrice TN, Ringli C, Muschietti JP (2017) RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358:1600–1603

    Article  CAS  PubMed  Google Scholar 

  • Meng D, Gu Z, Yuan H, Wang A, Li W, Yang Q, Zhu Y, Li T (2014) The microtubule cytoskeleton and pollen tube golgi vesicle system are required for in vitro S-RNase internalization and gametic self-incompatibility in apple. Plant Cell Physiol 55:977–989

    Article  CAS  PubMed  Google Scholar 

  • Miao HX, Ye ZX, Qin YH, Hu GB (2013) Identification of differentially expressed genes in 72B h styles from self-incompatible Citrus reticulata. Sci Hortic 161:278–285

    Article  CAS  Google Scholar 

  • Mondragon M, Johnarputharaj A, Pallmann M, Dresselhaus T (2017) Similarities between reproductive and immune pistil transcriptomes of Arabidopsis species. Plant Physiol 174:1559–1575

    Article  CAS  Google Scholar 

  • Ndinyanka TF, Vogler H, Draeger C, Munglani G, Gupta S, Herger AG, Knox JP, Grossniklaus U, Ringli C (2017) LRX Proteins play a crucial role in pollen grain and pollen tube cell wall development. Plant Physiol 176:1981–1992

    Google Scholar 

  • Pratas MI, Aguiar B, Vieira J, Nunes V, Teixeira V, Fonseca NA, Iezzoni A, van Nocker S, Vieira CP (2018) Inferences on specificity recognition at the Malusxdomestica gametophytic self-incompatibility system. Sci Rep 8:1717

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qu H, Zhang Z, Wu F, Wang Y (2016) The role of Ca2+ and Ca2+ channels in the gametophytic self-incompatibility of Pyrus pyrifolia. Cell Calcium 60:299–308

    Article  CAS  PubMed  Google Scholar 

  • Qu H, Guan Y, Wang Y, Zhang S (2017) PLC-mediated signaling pathway in pollen tubes regulates the gametophytic self-incompatibility of Pyrus species. Front Plant Sci 8:1164

    Article  PubMed  PubMed Central  Google Scholar 

  • 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:e84286

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sequeira L (1978) Lectins and their role in host-pathogen specificity. Annu Rev Phytopathol 16:453–481

    Article  CAS  PubMed  Google Scholar 

  • Shi D, Chao T, Wang R, Chao G, Xiao W, Shi H, Jin J, Zhang S (2017) Transcriptome and phytohormone analysis reveals a comprehensive phytohormone and pathogen defence response in pear self-/cross-pollination. Plant Cell Rep 36:1–15

    Article  CAS  Google Scholar 

  • Shulaev V, Korban SS, Sosinski B, Abbott AG, Aldwinckle HS, Folta KM, Iezzoni A, Main D, Arús P, Dandekar AM (2008) Multiple models for rosaceae genomics. Plant Physiol 147:985–1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Zhang S (2011) A cascade signal pathway occurs in self-incompatibility of Pyrus pyrifolia. Plant Signal Behav 6:420–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C-L, Wu J, Xu G-H, Gao Y-B, Chen G, Wu J-Y, Wu H-Q, Zhang S-L (2010a) S-RNase disrupts tip-localized reactive oxygen species and induces nuclear DNA degradation in incompatible pollen tubes of Pyrus pyrifolia. J Cell Sci 123:4301–4309

    Article  CAS  PubMed  Google Scholar 

  • Wang HJ, Huang JC, Jauh GY (2010b) Pollen germination and tube growth. Adv Bot Res 54:1–52

    Article  CAS  Google Scholar 

  • Wang GM, Gu C, Qiao X, Zhao BY, Ke YQ, Guo BB, Hao PP, Qi KJ, Zhang SL (2017) Characteristic of pollen tube that grew into self style in pear cultivar and parent assignment for cross-pollination. Sci Hortic 216:226–233

    Article  CAS  Google Scholar 

  • Wilkins KA, Poulter NS, Franklin-Tong VE (2014) Taking one for the team: self-recognition and cell suicide in pollen. J Exp Bot 65:1331–1342

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Zhang S, Wu J, Wang Y, Wu J (2007) Mutational mechanism of self-compatible pear cultivar‘jinzhuili’ (Pyrus bretschneideri). Acta Hortic Sin 34:295–300

    CAS  Google Scholar 

  • Wu JZ, Lin Y, Zhang XL, Pang DW, Zhao J (2008) IAA stimulates pollen tube growth and mediates the modification of its wall composition and structure in Torenia fournieri. J Exp Bot 59:2529–2543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Li M, Li T (2013a) Genetic features of the spontaneous self-compatible mutant ‘Jin Zhui’(Pyrus bretschneideri Rehd.). PLoS ONE 8:e76509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi K, Huang X, Wang Y, Zhao X, Deng C, Gou C, Zhou W, Yin H, Qin G, Sha Y, Tao Y, Chen H, Yang Y, Song Y, Zhan D, Wang J, Li L, Dai M, Gu C, Shi D, Wang X, Zhang H, Zeng L, Zheng D, Wang C, Chen M, Wang G, Xie L, Sovero V, Sha S, Huang W, Zhang M, Sun J, Xu L, Li Y, Liu X, Li Q, Shen J, Paull RE, Bennetzen JL (2013b) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yi M, Horton JD, Cohen J, Hobbs HH, Stephens RM (2006) WholePathwayScope: a comprehensive pathway-based analysis tool for high-throughput data. BMC Bioinform 7:30

    Article  CAS  Google Scholar 

  • Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309

    Article  CAS  PubMed  Google Scholar 

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Funding

Doctoral Fund of Qingdao Agricultural University, Integrated research and demonstration on reducing fertilizer and pesticide technology in Pear and peach trees (Grant No. 2018YFD0201400).

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QHY: Conceived and designed the experiments. KL: Performed the experiments. WYZ: Analyzed the data. QHY: Wrote the paper.

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Correspondence to Haiyong Qu.

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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 102, 287–306 (2020). https://doi.org/10.1007/s11103-019-00948-1

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