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Caspase-like proteases and the phytohormone cytokinin as determinants of S-RNAse–based self-incompatibility–induced PCD in Petunia hybrida L.

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Abstract

S-RNAse–based self-incompatibility (SI) in petunia (Petunia hybrida L.) is a self-/non-self-recognition system underlying the pistil rejection of self-pollen. Using different methods, including a TUNEL assay, we have recently shown that programmed cell death (PCD) is a factor of the SI in petunia. Here, we show that the growth of self-incompatible pollen tubes in the style tissues during 4 h after pollination is accompanied by five–sixfold increase in a caspase-like protease (CLP) activity. Exogenous cytokinin (CK) inhibits the pollen tube growth and stimulates the CLP activity in compatible pollen tubes. The actin depolymerization with latrunculin B induces a sharp drop in the CLP activity in self-incompatible pollen tubes and its increase in compatible pollen tubes. Altogether, our results suggest that a CLP is involved in the SI-induced PCD and that CK is a putative activator of the CLP. We assume that CK provokes acidification of the cytosol and thus promotes the activation of a CLP. Thus, our results suggest that CK and CLP are involved in the S-RNAse–based SI-induced PCD in petunia. Potential relations between these components in PCD signaling are discussed.

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References

  • Alallaq S, Ranjan A, Brunoni F, Novák O, Lakehal A, Bellini C (2020) Light controls de novo adventitious root regeneration by modulating jasmonate and cytokinin homeostasis in Norway spruce hypocotyls. bioRxivhttps://doi.org/10.1101/2020.03.11.985838

  • Andreev IM, Timofeeva GV, Minkina YV, Kovaleva LV (2007) Effects of exogenous phytohormones on intracellular pH of Petunia hybrida pollen grains. Russ J Plant Physiol 54(5):626–632

    CAS  Google Scholar 

  • Atkin-Smith GK, Poon IKH (2017) Disassembly of the dying: mechanisms and functions. Trends Cell Biol 27(2):151–162

    CAS  PubMed  Google Scholar 

  • Bonneau L, Ge Y, Drury GE, Gallois P (2008) What happened to plant caspases? J Exp Bot 59:491–499

    CAS  PubMed  Google Scholar 

  • Bosch M, Franklin-Tong VE (2007) Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in Papaver pollen. Proc Natl Acad Sci U S A 104:8327–1832

    Google Scholar 

  • Bosch M, Poulter NS, Vatovec S, Franklin-Tong VE (2008) Initiation of programmed cell death in self-incompatibility: role for cytoskeleton modifications and several caspase-like activities. Mol Plant 1:879–887

    CAS  PubMed  Google Scholar 

  • Bozhkov PV, Filonova LH, Suarez MF, Helmersson A, Smertenko AP, Zhivotovsky B, von Arnold S (2004) VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Differ 11:175–182

    CAS  PubMed  Google Scholar 

  • Bramhall S, Noack N, Wu M, Lowenberg J (1969) A simple colorimetric method for determination of protein. Anal Biochem 131(1-3):146–148

    Google Scholar 

  • Carimi F, Zottini M, Formentin E, Terzi M, Lo Schiavo F (2003) Cytokinins: new apoptotic inducers in plants. Planta 216(3):413–421

    CAS  PubMed  Google Scholar 

  • Carimi F, Terzi M, De Michele R, Zottini M, Lo Schiavo F (2004) High levels of the cytokinin BAP induce PCD by accelerating senescence. Plant Sci 166:963–969

    CAS  Google Scholar 

  • Carimi F, Zottini M, Costa A, Cattelan I, De Michele R, Terzi M, Lo SF (2005) NO signalling in cytokinin-induced programmed cell death. Plant, Cell and Environment 28:1171–1178

    CAS  Google Scholar 

  • Chen S, Jia J, Cheng L, Zhao P, Qi D, Yang W, Liu H, Dong X, Li X, Liu G (2019) Transcriptomic analysis reveals a comprehensive calcium-and phytohormone-dominated signaling response in Leymus chinensis self-incompatibility. Inter J Mol Sci 20(9):2356

    CAS  Google Scholar 

  • Choi J, Choi D, Lee S, Ryu CM, Hwang I (2011) Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci 16(7):388–394

    CAS  PubMed  Google Scholar 

  • Cortleven A, Schmülling T (2015) Regulation of chloroplast development and function by cytokinin. J Exp Bot 66(16):4999–5013

    CAS  PubMed  Google Scholar 

  • Danon A, Rotari VI, Gordon A, Mailhac N, Gallois P (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and defender against apoptotic death. J Biol Chem 279:779–787

    CAS  PubMed  Google Scholar 

  • Del Duca S, Aloisi I, Parrotta L, Cai G (2019) Cytoskeleton, transglutaminase and gametophytic self-incompatibility in the Malinae (Rosaceae). Inter J Mol Sci 20(1):209

    Google Scholar 

  • Del Pozo O, Lam E (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 8:1129–1132

    PubMed  Google Scholar 

  • Dickman M, Williams B, Li Y, de Figueiredo P, Wolpert T (2017) Reassessing apoptosis in plants. Nature plants 3(10):773–779

    CAS  PubMed  Google Scholar 

  • Duan H, Li Y, Pei Y, Deng W, Luo M, Xiao Y, Zhao D (2006) Auxin, cytokinin and ascisic acid: biosynthetic and catabolic genes and their potential applications in ornamental crops. J Crop Improvement 18(1–2):347–364

    CAS  Google Scholar 

  • Duan Z, Dou S, Liu Z, Li B, Yi B, Shen J, Ma C (2020) Comparative phosphoproteomic analysis of compatible and incompatible pollination in Brassica napus L. Acta Biochim Biophys Sin 52(4):446–456

    CAS  PubMed  Google Scholar 

  • Entani T, Iwano M, Shiba H, Che FS, Isogai A, Takayama S (2003) Comparative analysis of the self-incompatibility (S) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity. Genes Cells 8:203–213

    CAS  PubMed  Google Scholar 

  • Favaloro B, Allocanti N, Graziano V et al (2012) Role of apoptosis in disease. Aging 4:330–349

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Annicchiarico-Petruzzelli M (2018) Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death & Differentiation 25(3):486–541

    Google Scholar 

  • Ge Y, Cai YM, Bonneau L, Rotari V, Danon A, McKenzie EA, McLellan H, Mach L, Gallois P (2016) Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in Arabidopsis. Cell Death Differ 23(9):1493–1501

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vazquez-Santana S, Kim S, Phillips TE, Cruz-Garcia F, McClure B (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439:805–810

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hönig M, Plíhalová L, Husičková A, Nisler J, Doležal K (2018) Role of cytokinins in senescence, antioxidant defence and photosynthesis. Inter J Mol Sci 19(12):4045

    Google Scholar 

  • Hua Z, Kao T-h (2008) Identification of major lysine residues of S (3)-RNase of Petunia inflata involved in ubiquitin-26S proteasome-mediated degradation in vitro. Plant J 54:1094–1104

    CAS  PubMed  Google Scholar 

  • Hua Z, Vierstra RD (2011) The cullin-RING ubiquitin-protein ligases. Annu Rev Plant Biol 62:299–334

    CAS  PubMed  Google Scholar 

  • Hua Z, Meng X, Kao T- h (2007) Comparison of Petunia inflata S-Locus F-box protein (Pi SLF) with Pi SLF-like proteins reveals its unique function in S-RNase-based self-incompatibility. Plant Cell 19:3593–3609

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ishii Y, Hori Y, Sakai S, Honma Y (2002) Control of differentiation and apoptosis of human myeloid leukemia cells by cytokinins and cytokinin nucleosides, plant redifferentiation-inducing hormones. Cell Growth Differ 13(1):19–26

    CAS  PubMed  Google Scholar 

  • Iwano M, Takayama S (2012) Self/non-self discrimination in angiosperm self-incompatibility. Curr Opin Plant Biol 15(1):78–83

    PubMed  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

    CAS  Google Scholar 

  • Kovaleva LV, Zakharova EV, Minkina YV, Voronkov AS (2009) Effects of flavonols and phytohormones on germination and growth of petunia male gametophyte. Allelopathy J 23(1):51–62

    Google Scholar 

  • Kovaleva LV, Voronkov AS, Zakharova EV (2015) Role of auxin and cytokinin in the regulation of the actin cytoskeleton in the in vitro germinating male gametophyte of petunia. Russ J Plant Physiol 62(2):179–186

    CAS  Google Scholar 

  • Kovaleva L, Voronkov A, Zakharova E, Minkina Y, Timofeeva G, Andreev I (2016) Regulation of petunia pollen tube growth by phytohormones: identification of their potential targets. J Agric Sci Technol A 6:239–254

    CAS  Google Scholar 

  • Kovaleva LV, Zakharova EV, Timofeeva GV, Andreev IM, Golivanov YY, Bogoutdinova LR, Baranova EN, Khaliluev MR (2020) Aminooxyacetic acid (АОА), inhibitor of 1-aminocyclopropane-1-carboxilic acid (AСС) synthesis, suppresses self-incompatibility-induced programmed cell death in self-incompatible Petunia hybrida L. pollen tubes. Protoplasma 257:213–227

    CAS  PubMed  Google Scholar 

  • Kubo KI, Entani T, Takara A, Wang N, Fields AM, Hua Z, Toyoda M, Kawashima SI, Ando T, Isogai A, Kao TH, Takayama S (2010) Collaborative non-self-recognition system in S-RNase-based self-incompatibility. Science 330:796–799

    CAS  PubMed  Google Scholar 

  • Kubo K, Paape T, Hatakeyama M et al (2015) Gene duplication and genetic exchange drive the evolution of S-RNAse-based self-incompatibility in Petunia. Nat Plants 1:1–9

    Google Scholar 

  • Kubo KI, Tsukahara M, Fujii S, Murase K, Wada Y, Entani T, Iwano M, Takayama S (2016) Cullin1-P is an essential component of non-self recognition system in self-incompatibility in Petunia. Plant Cell Physiol 57:2403–2416

    CAS  PubMed  Google Scholar 

  • Kunikowska A, Byczkowska A, Doniak M, Kaźmierczak A (2013) Cytokinins résumé: their signaling and role in programmed cell death in plants. Plant Cell Rep 32(6):771–780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lai Z, Ma W, Han B, Liang L, Zhang Y, Hong G, Xue Y (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

    CAS  PubMed  Google Scholar 

  • Lam E, del Pozo O (2000) Caspase-like protease involvement in the control of plant cell death. Plant Mol Biol 44:417–428

    CAS  PubMed  Google Scholar 

  • Lee HS, Huang SS, Kao TH (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367:560–563

    CAS  PubMed  Google Scholar 

  • Li S, Sun P, Williams JS, T-h K (2014) Identification of the self-incompatibility locus F-box protein-containing complex in Petunia inflata. Plant Reprod 27:31–45

    PubMed  Google Scholar 

  • Lind JL, Bönig I, Clarke AE, Anderson MA (1996) A style-specific 120 kDa glycoprotein enters pollen tubes of Nicotiana alata in vivo. Sex Plant Reprod 9:75–86

    Google Scholar 

  • Liu W, Fan J, Li J et al (2014) SCFSLF-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

    PubMed  PubMed Central  Google Scholar 

  • Lord CE, Dauphinee AN, Watts RL, Gunawardena AH (2013) Unveiling interactions among mitochondria, caspase-like proteases, and the actin cytoskeleton during plant programmed cell death (PCD). PLoS One 8(3):e57110

    CAS  PubMed  PubMed Central  Google Scholar 

  • McClure B (2009) Darwin’s foundation for investigating self-incompatibility and the progress toward a physiological model for S-RNase-based SI. J Exp Bot 60:1069–1081

    CAS  PubMed  Google Scholar 

  • McClure BA, Gray JE, Anderson MA et al (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347:757–760

    CAS  Google Scholar 

  • Meng X, Hua Z, Sun P, Kao T-h (2011) The amino terminal F-box domain of Petunia inflata S-locus F-box protein is involved in the S-RNase-based self-incompatibility mechanism. AoB Plants plr016. https://doi.org/10.1093/aobpla/plr016

  • Mlejnek P, Procházka S (2002) Activation of caspase-like proteases and induction of apoptosis by isopentenyladenosine in tobacco BY-2 cells. Planta 215(1):158–166

    CAS  PubMed  Google Scholar 

  • Murfett J, Atherton TL, Mou B, Gassert CS, McClure BA (1994) S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367:563–566

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Parrish AB, Freel CD, Kornbluth S (2013) Cellular mechanisms controlling caspase activation and function. Cold Spring Harbor 5(6):a008672

    Google Scholar 

  • Qin Y, Yang Z (2011) Rapid tip growth: insights from pollen tubes. Semin Cell Dev Biol 22(8):816–824

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roalson EH, McCubbin AG (2003) S-RNases and sexual incompatibility: structure, functions, and evolutionary perspectives. Mol Phylogenet Evol 29:490–506

    CAS  PubMed  Google Scholar 

  • Roldán JA, Rojas HJ, Goldraij A (2012) Disorganization of F-actin cytoskeleton precedes vacuolar disruption in pollen tubes during the in vivo self-incompatibility response in Nicotiana alata. Ann Bot 110:787–795

    PubMed  PubMed Central  Google Scholar 

  • Romanov GA (2002) The phytohormone receptors. Russ J Plant Physiol 49(4):552–560

    CAS  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    CAS  PubMed  Google Scholar 

  • Sassa H (2016) Molecular mechanism of the S-RNase-based gametophytic self-incompatibility in fruit trees of Rosaceae. Breed Sci 66:116–121

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schaller GE, Bishopp A, Kieber JJ (2015) The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27(1):44–63

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi D, Tang C, Wang R, Gu C, Wu X, Hu S, Zhang S (2017) Transcriptome and phytohormone analysis reveals a comprehensive phytohormone and pathogen defence response in pear self−/cross-pollination. Plant Cell Rep 36(11):1785–1799

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao TH (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305

    CAS  PubMed  Google Scholar 

  • Singh A, Ai Y, Kao TH (1991) Characterization of ribonuclease activity of three S-allele-associated proteins of Petunia inflata. Plant Physiol 96:61–68

    CAS  PubMed  PubMed Central  Google Scholar 

  • Skalák J, Vercruyssen L, Claeys H, Hradilová J, Černý M, Novák O, Dhondt S (2019) Multifaceted activity of cytokinin in leaf development shapes its size and structure in Arabidopsis. Plant J 97(5):805–824

    PubMed  Google Scholar 

  • Smertenko A, Franklin-Tong VE (2011) Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death Differ 18:1263–1270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spinola M, Colombo F, Falvella FS, Dragani TA (2007) N6-isopentenyladenosine: a potential therapeutic agent for a variety of epithelial cancers. Inter J Cancer 120(12):2744–2748

    CAS  Google Scholar 

  • Staiger CJ, Poulter NS, Henty JL, Franklin-Tong VE, Blanchoin L (2010) Regulation of actin dynamics by actin-binding proteins in pollen. J Exp Bot 61:1969–1986

    CAS  PubMed  Google Scholar 

  • Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467–489

    CAS  PubMed  Google Scholar 

  • Thomas SG, Huang S, Li S, Staiger CJ, Franklin-Tong VE (2006) Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. J Cell Biol 174:221–229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tixeira R, Poon IKH (2019) Disassembly of dying cells in diverse organisms. Cell Mol Life Sci 76:245–257

    CAS  PubMed  Google Scholar 

  • van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:4749–4761

    PubMed  Google Scholar 

  • Van Hautegem Т, Waters AJ, Goodrich J et al (2015) Only in dying, life: programmed cell death during plant development. Trends Plant Sci 20:102–113

    PubMed  Google Scholar 

  • Vescovi M, Riefler M, Gessuti M, Novák O, Schmülling T, Lo SF (2012) Programmed cell death induced by high levels of cytokinin in Arabidopsis cultured cells is mediated by the cytokinin receptor CRE1/AHK4. J Exp Bot 63(7):2825–2832

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waidmann S, Kleine-Vehn J (2020) Asymmetric cytokinin signaling opposes gravitropism in roots. J Integrative Plant Biol 62(7):882–886

    CAS  Google Scholar 

  • Waidmann S, Rosquete MR, Schöller M, Sarkel E, Lindner H, La Rue T, Novak O (2019) Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots. Nat Commun 10(1):1–14

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wang X, McCubbin AG et al (2003) Genetic mapping and molecular characterization of the self-incompatibility (S) locus in Petunia inflata. Plant Mol Biol 53:565–580

    CAS  PubMed  Google Scholar 

  • Wang CL, Xu GY, Jiang XT et al (2009) S-RNase triggers mitochondrial alteration and DNA degradation in the incompatible pollen tube of Pyrus pyrifolia in vitro. Plant J 57(2):220–229

    CAS  PubMed  Google Scholar 

  • Wang CL, Wu J, Xu GH, Gao YB, Chen G, Wu JY, Wu HQ, Zhang SL (2010) 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

    CAS  PubMed  Google Scholar 

  • Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci U S A 98:10487–10492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15(11):2532–2550

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wheeler MJ, Vatovec S, Franklin-Tong VE (2010) The pollen S-determinant in Papaver: comparisons with known plant receptors and protein ligand partners. J Exp Bot 61:2015–2025

    CAS  PubMed  Google Scholar 

  • Wilkins KA, Bosch M, Haque T, Teng N, Poulter NS, Franklin-Tong VE (2015) Self-incompatibility-induced programmed cell death in field poppy pollen involves dramatic acidification of the incompatible pollen tube cytosol. Plant Physiol 167:766–779

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang QF, Li J, Bi FC, Liu Z, Chang ZY, Wang LY, Huang LQ, Yao N (2020) Ceramide-induced cell death depends on calcium and caspase-like activity in rice. Front Plant Sci 11:145

    PubMed  PubMed Central  Google Scholar 

  • Zhao L, Huang J, Zhao Z, Li Q, Sims TL, Xue Y (2010) The Skp1-like protein SSK1 is required for cross-pollen compatibility in S-RNase based self-incompatibility. Plant J 62:52–63

    CAS  PubMed  Google Scholar 

  • Zhou J, Lu M, Yu S, Liu Y, Yang J, Tan X (2020) In-depth understanding of Camellia oleifera self-incompatibility by comparative transcriptome, proteome and metabolome. Inter J Mol Sci 21(5):1600

    CAS  Google Scholar 

  • Zürcher E, Liu J, di Donato M, Geisler M, Müller B (2016) Plant development regulated by cytokinin sinks. Science 353(6303):1027–1030

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors express their deep gratitude to Azarkovich Marina Ivanovna (IPP RAS) for mastering the method of extraction and determination of proteins. The authors are grateful to Alexander Tyurin for his technical assistance and to the functional genomics Group (IPP RAS) headed by Irina Goldenkova-Pavlova for the opportunity to work on the equipment.

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E. Zakharova and L. Kovaleva conceived and designed the research, and wrote the manuscript; E. Zakharova, G. Timofeeva, and A. Fateev conducted the experiments.

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Correspondence to Ekaterina V. Zakharova.

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Zakharova, E.V., Timofeeva, G.V., Fateev, A.D. et al. Caspase-like proteases and the phytohormone cytokinin as determinants of S-RNAse–based self-incompatibility–induced PCD in Petunia hybrida L.. Protoplasma 258, 573–586 (2021). https://doi.org/10.1007/s00709-020-01587-w

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