Isobaric tags for relative and absolute quantitation-based quantitative proteomics analysis provides novel insights into the mechanism of cross-incompatibility between tree peony and herbaceous peony
Dan He A B , Xue-Yuan Lou A , Song-Lin He C D , Ya-Kai Lei A , Bo-Va Lv A , Zheng Wang A , Yun-Bing Zheng A and Yi-Ping Liu A
+ Author Affiliations
- Author Affiliations
A College of Forestry, Henan Agricultural University, Zhengzhou 450002, Henan, China.
B Henan Institute of Science and Technology, Postdoctor Researche Base, Xinxiang 453000, Henan, China.
C Henan Institute of Science and Technology, Xinxiang 453000, Henan, China.
D Corresponding author. Email: hsl213@yeah.net
Functional Plant Biology 46(5) 417-427 https://doi.org/10.1071/FP18163
Submitted: 20 June 2018 Accepted: 14 January 2019 Published: 12 February 2019
Abstract
Interspecific hybridisation is the main method for improvement and breeding of tree peony (Paeonia ostii T.Hong & J.X.Zhang), but cross-incompatibility as the major factor restricting the rapid development of interspecific hybridisation. To better understand the molecular mechanisms involved in cross-incompatibility between tree peony (Paeonia ostii cv. Fengdanbai) and herbaceous peony (Paeonia lactiflora Pall. cv. Fenyunu), a quantitative proteomic analysis using isobaric tags for relative and absolute quantitation (iTRAQ) technology was performed on the stigma 24 h after pollination. Of the 2900 proteins whose levels were quantitated, 685 proteins were differentially expressed in the stigma after hybrid pollination, in contrast to self-pollination. Functional annotation analysis showed that dysregulated proteins involved in RNA degradation, the Ca signalling pathway, the phosphatidylinositol signalling system and the mitogen-activated protein kinase (MAPK) signalling pathway may have made contributions to cross-incompatibility. The downregulated expression of enolase, DnaK (Heat Shock Proteins, HSP70), GroEL (Heat Shock Proteins, HSP60), calmodulin and glyoxalase I, and the upregulated expression of adenine nucleotide translocator indicated that the energy synthesis required by pollen tube growth, the signal pathway and the metabolic pathway related to the growth polarity of the pollen tube were blocked after hybrid pollination. Eight genes were selected to confirm their expression by quantitative real-time PCR. Compared with the STRING database, a protein–protein interaction network of the chosen proteins was constructed. These results provide fundamental and important information for research into the molecular mechanisms of cross-incompatibility in peony and should facilitate interspecific hybridisation in agricultural practice.
Additional keywords: interspecific hybridisation, iTRAQ, Paeonia ostii, Paeonia lactiflora.
References
Antonov AV, Dietmann S, Rodchenkov I, Mewes HW (2009) PPI spider: a tool for the interpretation of proteomics data in the context of protein–protein interaction networks. Proteomics 9, 2740–2749.| PPI spider: a tool for the interpretation of proteomics data in the context of protein–protein interaction networks.Crossref | GoogleScholarGoogle Scholar | 19405022PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. American Journal of Botany 50, 859–865.
| The essential role of calcium ion in pollen germination and pollen tube growth.Crossref | GoogleScholarGoogle Scholar |
Casado-Vela J, Martínez-Esteso MJ, Rodriguez E, Borrás E, Elortza F, Bru-Martínez R (2010) iTRAQ-based quantitative analysis of protein mixtures with large fold change and dynamic range. Proteomics 10, 343–347.
| iTRAQ-based quantitative analysis of protein mixtures with large fold change and dynamic range.Crossref | GoogleScholarGoogle Scholar | 20029838PubMed |
Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410, 37–40.
| Mammalian MAP kinase signalling cascades.Crossref | GoogleScholarGoogle Scholar | 11242034PubMed |
Chu P, Yan GX, Yang Q, Zhai LN, Zhang C, Zhang FQ, Guan RZ (2015) iTRAQ-based quantitative proteomics analysis of Brassica napus leaves reveals pathways associated with chlorophyll deficiency. Proteomics 113, 244–259.
| iTRAQ-based quantitative proteomics analysis of Brassica napus leaves reveals pathways associated with chlorophyll deficiency.Crossref | GoogleScholarGoogle Scholar | 25317966PubMed |
Gachon C, Mingam A, Charrier B (2004) Real-time PCR: what relevance to plant studies? Journal of Experimental Botany 55, 1445–1454.
| Real-time PCR: what relevance to plant studies?Crossref | GoogleScholarGoogle Scholar | 15208338PubMed |
Grunberg-Manago M (1999) Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annual Review of Genetics 33, 193–227.
| Messenger RNA stability and its role in control of gene expression in bacteria and phages.Crossref | GoogleScholarGoogle Scholar | 10690408PubMed |
Guan Y, Guo J, Li H, Yang Z (2013) Signaling in pollen tube growth: crosstalk, feedback, and missing links. Molecular Plant 6, 1053–1064.
| Signaling in pollen tube growth: crosstalk, feedback, and missing links.Crossref | GoogleScholarGoogle Scholar | 23873928PubMed |
Haig D, Westoby M (1991) Genomic imprinting in endosperm: its effect on seed development in crosses between species, and between different ploidies of the same species, and its implications for the evolution of apomixis. Philosophical Transactions: Biological Sciences 333, 1–13.
| Genomic imprinting in endosperm: its effect on seed development in crosses between species, and between different ploidies of the same species, and its implications for the evolution of apomixis.Crossref | GoogleScholarGoogle Scholar |
Harmon AC, Gribskov M, Harper JF (2000) CDPKs – a kinase for every Ca2+ signal? Trends in Plant Science 5, 154–159.
| CDPKs – a kinase for every Ca2+ signal?Crossref | GoogleScholarGoogle Scholar | 10740296PubMed |
Hashimoto H, Nishi R, Umeda M, Uchimiya H, Kato A (1993) Isolation and characterization of a rice cDNA clone encoding ATP/ADP translocator. Plant Molecular Biology 22, 163–164.
| Isolation and characterization of a rice cDNA clone encoding ATP/ADP translocator.Crossref | GoogleScholarGoogle Scholar | 8499614PubMed |
He D, Li R, Ji SY, Wu J, Wang Z, Liu YP, He SL (2014) Cloning and expression analysis of adventitious rooting related gene PsARRO-1 of tree peony. Chih Wu Sheng Li Hsueh T’ung Hsun 50, 1151–1158.
Ischebeck T, Stenzel I, Heilmann I (2008) Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion. The Plant Cell 20, 3312–3330.
| Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion.Crossref | GoogleScholarGoogle Scholar | 19060112PubMed |
Kao TH, McCubbin AG (1996) How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proceedings of the National Academy of Sciences of the United States of America 93, 12059–12065.
| How flowering plants discriminate between self and non-self pollen to prevent inbreeding.Crossref | GoogleScholarGoogle Scholar | 8901531PubMed |
Kho YO, Baër J (1968) Observing pollen tubes by means of fluorescence. Euphytica 17, 298–302.
Lal SK, Johnson S, Conway T, Kelley PM (1991) Characterization of a maize cDNA that complements an enolase-deficient mutant of Escherichia coli. Plant Molecular Biology 16, 787–795.
| Characterization of a maize cDNA that complements an enolase-deficient mutant of Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1859865PubMed |
Lan P, Li W, Wen TN, Shiau JY, Wu YC, Lin W, Schmidt W (2011) iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis. Plant Physiology 155, 821–834.
| iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis.Crossref | GoogleScholarGoogle Scholar | 21173025PubMed |
Landry SJ, Jordan R, McMacken R, Gierasch LM (1992) Different conformations for the same polypeptide bound to chaperones DnaK and GroEL. Nature 355, 455–457.
| Different conformations for the same polypeptide bound to chaperones DnaK and GroEL.Crossref | GoogleScholarGoogle Scholar | 1346469PubMed |
Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. The EMBO Journal 21, 2692–2702.
| LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase.Crossref | GoogleScholarGoogle Scholar | 12032082PubMed |
Li S, Samaj J, Franklin-Tong VE (2007) A mitogen-activated protein kinase signals to programmed cell death induced by self-incompatibility in Papaver pollen. Plant Physiology 145, 236–245.
| A mitogen-activated protein kinase signals to programmed cell death induced by self-incompatibility in Papaver pollen.Crossref | GoogleScholarGoogle Scholar | 17660353PubMed |
Lowry DB, Modliszewski JL, Wright KM, Wu CA, Willis JH (2008) The strength and genetic basis of reproductive isolating barriers in flowering plants. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 3009–3021.
| The strength and genetic basis of reproductive isolating barriers in flowering plants.Crossref | GoogleScholarGoogle Scholar | 18579478PubMed |
Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. The Plant Cell 14, S389–S400.
| Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants.Crossref | GoogleScholarGoogle Scholar | 12045290PubMed |
Malho R, Trewavas AJ (1996) Localized apical increases of cytosolic free calcium control pollen tube orientation. The Plant Cell 8, 1935–1949.
| Localized apical increases of cytosolic free calcium control pollen tube orientation.Crossref | GoogleScholarGoogle Scholar | 12239370PubMed |
Martin P (1997) ‘The gardener’s guide to growing peonies.’ (Timber Press Inc.: Portland, OR)
McClure BA, Gray JE, Anderson MA, Clarke AE (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347, 757–760.
| Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA.Crossref | GoogleScholarGoogle Scholar |
Monteiro D, Liu Q, Lisboa S, Scherer GE, Quader H, Malhó R (2005) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion. Journal of Experimental Botany 56, 1665–1674.
| Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion.Crossref | GoogleScholarGoogle Scholar | 15837704PubMed |
Nogueira FC, Palmisano G, Schwämmle V, Campos FA, Larsen MR, Domont GB, Roepstorff P (2012) Performance of isobaric and isotopic labeling in quantitative plant proteomics. Journal of Proteome Research 11, 3046–3052.
| Performance of isobaric and isotopic labeling in quantitative plant proteomics.Crossref | GoogleScholarGoogle Scholar | 22452248PubMed |
Py B, Higgins CF, Krisch HM, Carpousis AJ (1996) A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381, 169–172.
| A DEAD-box RNA helicase in the Escherichia coli RNA degradosome.Crossref | GoogleScholarGoogle Scholar | 8610017PubMed |
Qin Y, Yang Z (2011) Rapid tip growth: insights from pollen tubes. Seminars in Cell & Developmental Biology 22, 816–824.
| Rapid tip growth: insights from pollen tubes.Crossref | GoogleScholarGoogle Scholar |
Rato C, Monteiro D, Hepler PK, Malhó R (2004) Calmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes. The Plant Journal 38, 887–897.
| Calmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes.Crossref | GoogleScholarGoogle Scholar | 15165182PubMed |
Rudd JJ, Osman K, Franklin FC, Franklin-Tong VE (2003) Activation of a putative MAP kinase in pollen is stimulated by the self-incompatibility (SI) response. FEBS Letters 547, 223–227.
| Activation of a putative MAP kinase in pollen is stimulated by the self-incompatibility (SI) response.Crossref | GoogleScholarGoogle Scholar | 12860418PubMed |
Sang T, Crawford DJ, Stuessy TF (1995) Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proceedings of the National Academy of Sciences of the United States of America 92, 6813–6817.
| Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution.Crossref | GoogleScholarGoogle Scholar | 7624325PubMed |
Schmittgen DT, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101–1108.
| Analyzing real-time PCR data by the comparative CT method.Crossref | GoogleScholarGoogle Scholar |
Sheoran IS, Pedersen EJ, Ross AR, Sawhney VK (2009) Dynamics of protein expression during pollen germination in canola (Brassica napus). Planta 230, 779–793.
| Dynamics of protein expression during pollen germination in canola (Brassica napus).Crossref | GoogleScholarGoogle Scholar | 19629521PubMed |
Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, Keating SP, Hunter CL, Nuwaysir LM, Schaeffer DA (2007) The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Molecular & Cellular Proteomics 6, 1638–1655.
| The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra.Crossref | GoogleScholarGoogle Scholar |
Singla-Pareek SL, Reddy MK, Sopory SK (2003) Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance. Proceedings of the National Academy of Sciences of the United States of America 100, 14672–14677.
| Genetic engineering of the glyoxalase pathway in tobacco leads to enhanced salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 14638937PubMed |
Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytologist 151, 35–66.
| Calmodulin as a versatile calcium signal transducer in plants.Crossref | GoogleScholarGoogle Scholar |
Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecology Letters 6, 1025–1037.
| The evolutionary and ecological role of heat shock proteins.Crossref | GoogleScholarGoogle Scholar |
Sousa E, Kost B, Malhó R (2008) Arabidopsis phosphatidylinositol-4-monophosphate 5-kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling. The Plant Cell 20, 3050–3064.
| Arabidopsis phosphatidylinositol-4-monophosphate 5-kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling.Crossref | GoogleScholarGoogle Scholar | 19033528PubMed |
Stern FC (1946) ‘A study of the genus Paeonia.’ (The Royal Horticultural Society: London)
Su PH, Li HM (2008) Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiology 146, 1231–1241.
| Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds.Crossref | GoogleScholarGoogle Scholar | 18192441PubMed |
Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, Mering C (2015) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Research 43, D447–D452.
| STRING v10: protein–protein interaction networks, integrated over the tree of life.Crossref | GoogleScholarGoogle Scholar | 25352553PubMed |
Tonosaki K, Osabe K, Kawanabe T, Fujimoto R (2016) The importance of reproductive barriers and the effect of allopolyploidization on crop breeding. Breeding Science 66, 333–349.
| The importance of reproductive barriers and the effect of allopolyploidization on crop breeding.Crossref | GoogleScholarGoogle Scholar | 27436943PubMed |
Wister JC (1928) The mountain tree peony. In ‘Peonies’. (Ed. J Boyd) pp. 219–244. (American Horticultural Society, Washington, DC)
Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends in Plant Science 8, 505–512.
| Calcium/calmodulin-mediated signal network in plants.Crossref | GoogleScholarGoogle Scholar | 14557048PubMed |
Zhao Y, Yan A, Feijó JA, Furutani M, Takenawa T, Hwang I, Fu Y, Yang Z (2010) Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco. The Plant Cell 22, 4031–4044.
| Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco.Crossref | GoogleScholarGoogle Scholar | 21189293PubMed |
