Abstract
The polyamine (PA) content and the transglutaminase (TGase) activity have been investigated in Pyrus communis pollination with compatible and self-incompatible (SI) pollen in order to deepen their possible involvement in the progamic phase of plant reproduction. The PA distribution as free, perchloric acid (PCA)-soluble and PCA-insoluble fractions in ungerminated (UGP), germinating pollen (GP), styles and pollinated styles with compatible and SI pollens is discussed in the light of a possible role during pollination. Generally, the conjugated PAs both in PCA-soluble and PCA-insoluble fractions were higher than the free form. Within the conjugated PAs, the PCA-insoluble ones were the highest with the exception of the not pollinated styles. As TGase mediates some of the effects of PAs by covalently binding them to proteins, the activity of this enzyme, never checked before in styles and pollinated styles, was examined. In the SI styles, the TGase activity is higher in comparison to style-pollinated with compatible pollen, and high molecular mass cross-linked products were formed, suggesting an involvement of TGase in SI response. This is the first evidence on the presence of this enzyme activity in not pollinated and pollinated styles.
Similar content being viewed by others
Abbreviations
- PAs:
-
Aliphatic polyamines
- PU:
-
Putrescine
- SD:
-
Spermidine
- SM:
-
Spermine
- TGase:
-
Transglutaminase
- GP:
-
Germinating pollen
- UGP:
-
Ungerminated pollen
- SI:
-
Self-incompatibility
- PCA:
-
Perchloric acid
References
Altman A (2006) Polyamines and wounded storage tissues—inhibition of RNase activity and solute leakage. Physiol Plant 54:194–198
Antognoni F, Bagni N (2008) Bis(guanylhydrazones) negatively affect in vitro germination of kiwifruit pollen and alter the endogenous polyamine pool. Plant Biol 10:334–341
Bagni N, Pistocchi R (1990) Binding, transport and subcellular compartmentation of polyamines in plants. In: Flores HE, Arteca RN, Shannon JC (eds) Polyamines and ethylene: biochemistry, physiology and interactions. American Society of Plant Physiology, Rockville, pp 62–72
Bagni N, Adamo P, Serafini-Fracassini D, Villanueva VR (1981) RNA, proteins and polyamines during tube growth in germinating apple pollen. Plant Physiol 68:727–730
Biasi R, Falasca G, Altamura MM, Fabbri S, Bagni N (1997) Reproductive morphogenesis in kiwifruit in relation to polyamines. Acta Horticul 444:479–484
Biasi R, Falasca G, Speranza A, De Stradis A, Scoccianti V, Franceschetti M, Bagni N, Altamura MM (2001) Biochemical and ultrastructural features related to male sterility in the dioecious species Actinidia deliciosa. Plant Physiol Biochem 39:395–406
Bokern M, Witte L, Wray V, Nimtz M, Meurer-Grimes B (1995) Trisubstituted hydroxycinnamic acid Spds from Quercus dentata pollen. Phytochem 39:1371–1375
Brown RE, Jarvis KL, Hyland KJ (1989) Protein measurement using bicinchoninic acid: elimination of interfering substances. Anal Biochem 180:136–139
Cai G, Romagnoli S, Moscatelli A, Ovidi E, Gambellini G, Tiezzi A, Cresti M (2000) Identification and characterization of a novel microtubule-based motor associated with membranous organelles in tobacco pollen tubes. Plant Cell 12:1719–1736
Capell T, Claparols I, Del Duca S, Bassie L, Miro B, Rodriguez-Montesinos J, Christou P, Serafini-Fracassini D (2004) Producing transglutaminases by molecular farming in plants: minireview article. Amino Acids 26:419–423
Chibi F, Matilla A, Angosto T, Garrido D (1994) Changes in polyamine synthesis during anther development and pollen germination in tobacco (Nicotiana tabacum). Physiol Plant 92:61–68
Del Duca S, Bregoli AM, Bergamini C, Serafini-Fracassini D (1997) Transglutaminase-catalyzed modification of cytoskeletal proteins by polyamines during the germination of Malus domestica pollen. Sex Plant Reprod 10:89–95
Del Duca S, Serafini-Fracassini D, Bonner PLR, Cresti M, Cai G (2009) Effects of post-translational modifications catalyzed by pollen transglutaminase on the functional properties of microtubules and actin filaments. Biochem J 418:651–664
Della Mea M, De Filippis F, Genovesi V, Serafini-Fracassini D, Del Duca S (2007a) The acropetal wave of developmental cell death (DCD) of Nicotiana tabacum corolla is preceded by activation of transglutaminase in different cell compartments. Plant Physiol 144:1–13
Della Mea M, Serafini-Fracassini D, Del Duca S (2007b) Programmed cell death: similarities and differences in animals and plants. A flower paradigm. Amino Acids 33:395–404
Grienenberger E, Besseau S, Geoffroy P, Debayle D, Heintz D, Lapierre C, Pollet B, Heitz T, Legrand M (2009) A BAHD acyltransferase is expressed in the tapetum of Arabidopsis anthers and is involved in the synthesis of hydroxycinnamoyl spermidines. Plant J 58:246–259
Griffin M, Casadio R, Bergamini CM (2002) Transglutaminases: nature’s biological glues. Biochem J 368:377–396
Ientile R, Caccamo D, Griffin M (2007) Tissue transglutaminase and the stress response. Amino Acids 33:385–394
Kotsakis P, Griffin M (2007) Tissue transglutaminase in tumour progression: friend or foe? Amino Acids 33:373–384
Lam TBT, Iiyama K, Stone B (1992) Cinnamic acid bridges between cell wall polymers in wheat and Phalaris internodes. Phytochem 31:1179–1183
Lilley GR, Skill J, Griffin M, Bonner PL (1998) Detection of Ca2+-dependent transglutaminase activity in root and leaf tissue of monocotyledonous and dicotyledonous plants. Plant Physiol 117:1115–1123
Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4:140–156
Martin-Tanguy J, Perdrizet E, Prevost J, Martin C (1982) The distribution of hydroxycinnamic acid amides in fertile and cytoplasmic male sterile lines of maize. Phytochem 21:1939–1945
McClure BA, Franklin-Tong V (2006) Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition. Planta 224:233–245
Persia D, Cai G, Del Casino C, Faleri C, Willemse MT, Cresti M (2008) Sucrose synthase is associated with the cell wall of tobacco pollen tubes. Plant Physiol 147:1603–1618
Pohjanpelto P, Virtanen I, Holtta E (1981) Polyamine starvation causes disappearance of actin filaments and microtubules in polyamine-auxotrophic cells. Nature 293:475–477
Robinson NJ, Baker PN, Jones CJ, Aplin JD (2007) A role for tissue transglutaminase in stabilization of membrane-cytoskeletal particles shed from the human placenta. Biol Reprod 77:648–657
Scaramagli S, Bueno M, Torrigiani P, Altamura MM, Capitani F, Bagni N (1995) Morphogenesis in cultured thin layers and pith explants of tobacco. II. Early hormone modulated polyamine biosynthesis. J Plant Physiol 147:113–117
Serafini-Fracassini D (1991) Cell cycle-dependent changes in plant polyamine metabolism. In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants. CRC Press, Boca Raton, pp 175–186
Serafini-Fracassini D, Del Duca S, D’Orazi D (1988) First evidence for polyamine conjugation mediated by an enzymic activity in plants. Plant Physiol 87:757–761
Serafini-Fracassini D, Della Mea M, Tasco G, Casadio R, Del Duca S (2009) Plant and animal transglutaminases: do similar functions imply similar structures? Amino Acids 36:643–657
Speranza A, Calzoni GL, Bagni N (1984) Evidence for a polyamine-mediated control of ribonuclease activity in germinating pollen. Physiol Veg 22:323–331
Thomas V, Fournet G, Simonet F, Roch AM, Ceylan I, El Alaouia S, Quash G (2004) Definition of the fine specificity of the monoclonal antibody 81D4: its reactivity with lysine and polyamine isopeptide cross-links. J Immunol Methods 292:83–95
Waffenschmidt S, Kusch T, Woessner JP (1999) A transglutaminase immunologically related to tissue transglutaminase catalyses cross-linking of cell wall proteins in Chlamydomonas reinhardtii. Plant Physiol 121:1003–1015
Acknowledgments
Thanks are due to the Italian Ministero dell’Università that supported this work by a grant to DSF, Dipartimento Biologia Evoluzionistica Sperimentale, University of Bologna (PRIN 2007, http://prin.miur.it/). Many thanks to Dr. F. Antognoni for valuable scientific discussion and Dr. C. Pagnucco for her technical assistance.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Del Duca, S., Cai, G., Di Sandro, A. et al. Compatible and self-incompatible pollination in Pyrus communis displays different polyamine levels and transglutaminase activity. Amino Acids 38, 659–667 (2010). https://doi.org/10.1007/s00726-009-0426-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-009-0426-5