Ethylene-dependent effects on generative organ abscission of Lupinus luteus

Kamil Frankowski, Agata Kućko, Agnieszka Zienkiewicz, Krzysztof Zienkiewicz, Juan de Dios Alché, Jan Kopcewicz, Emilia Wilmowicz

Abstract


The abscission of certain organs from the plant is part of the fulfilment of its developmental programs. The separation process occurs in a specialized abscission zone usually formed at the base of detached organ. The changing level of phytohormones, particularly ethylene, is the element responsible for coordinating anatomical and physiological transformation that accompanies organ abscission. The application of ethylene (ET) on Lupinus luteus stimulates flower abortion. However, the treatment with 1-aminocyclopropane-1-carboxylic acid (ACC) – direct ET precursor – does not cause such a strong physiological response. In turn, when applied on the pedicels both ET biosynthesis (2-aminoethoxyvinylglycine; AVG) and action (norbornadiene; NBD) inhibitors reversed the stimulatory effect of ET on generative organ separation. In order to determine ET role in the flower abscission process in L. luteus, we identified the sequences coding for synthase (LlACS) and oxidase (LlACO) of ACC and measured their expression levels. Abscission zone activation is accompanied by a considerable increase both in LlACS and LlACO cDNAs and also ACC content, which is specifically localized in the dividing cells at the base of the flower being detached. Obtained results suggest that ET is a strong stimulator of flower abortion in L. luteus.

Keywords


1-aminocyclopropane-1-carboxylic acid; ethylene; Lupinus luteus; phytohormones; organ abscission

Full Text:

PDF

References


Frankowski K, Wilmowicz E, Kućko A, Mączkowski R, Marciniak K, Kopcewicz J. The generative development of traditional and self-completing (restricted branching) cultivars of white lupine (Lupinus albus L.), yellow lupine (L. luteus L.) and narrow-leafed lupine (L. angustifolius L.) grown under different phytotron conditions. Plant Breeding and Seed Science. 2014;69:47–57. https://doi.org/10.1515/plass-2015-0005

Prusiński J, Borowska M. Degree of success of legume cultivars registered by the center for cultivar testing over the period of market economy. Acta Scientiarum Polonorum. Agricultura. 2001;6:3–16.

Estornell LH, Agustí J, Merelo P, Talón M, Tadeo FR. Elucidating mechanisms underlying organ abscission. Plant Sci. 2013;199–200:48–60. https://doi.org/10.1016/j.plantsci.2012.10.008

Taylor JE, Whitelaw CA. Signals in abscission. New Phytol. 2001;151:323–339. https://doi.org/10.1046/j.0028-646x.2001.00194.x

Roberts JA, Whitelaw CA, Gonzalez-Carranza ZH, McManus MT. Cell separation processes in plants – models, mechanisms and manipulation. Ann Bot. 2000;86(2):223–235. https://doi.org/10.1006/anbo.2000.1203

van Doorn WG. Effect of ethylene of flower abscission: a survey. Ann Bot. 2002;89(6):689–693. https://doi.org/10.1093/aob/mcf124

Yang SF, Hoffman NE. Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Physiol. 1984;35:155–189. https://doi.org/10.1146/annurev.pp.35.060184.001103

Kęsy J, Frankowski K, Wilmowicz E, Glazińska P, Wojciechowski W, Kopcewicz J. The possible role of PnACS2 in IAA-mediated flower inhibition in Pharbitis nil. Plant Growth Regul. 2010;61(1):1–10. https://doi.org/10.1007/s10725-010-9443-3

Sawicki M, Barka EA, Clément C, Vaillant-Gaveau N, Jacquard C. Cross-talk between environmental stresses and plant metabolism during reproductive organ abscission. J Exp Bot. 2015;66:1707–719. https://doi.org/10.1093/jxb/eru533

Wilmowicz E, Frankowski K, Kęsy J, Glazińska P, Wojciechowski W, Kućko A, et al. The role of PnACO1 in light- and IAA-regulated flower inhibition in Pharbitis nil. Acta Physiol Plant. 2013;35(3):801–810. https://doi.org/10.1007/s11738-012-1121-9

Wilmowicz E, Frankowski K, Kęsy J, Kućko A, Kopcewicz J. Involvement of the IAA-regulated ACC oxidase gene PnACO3 in Pharbitis nil flower inhibition. Acta Biol Crac Ser Bot. 2014;56(1):90–96. https://doi.org/10.2478/abcsb-2014-0013

Argueso CT, Hansen M, Kieber JJ. Regulation of ethylene biosynthesis. J Plant Growth Regul. 2007;26(2):92–105. https://doi.org/10.1007/s00344-007-0013-5

Belfield EJ, Ruperti B, Roberts JA, McQueen-Mason S. Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra. J Exp Bot. 2005;56(413):817–823. https://doi.org/10.1093/jxb/eri076

Frankowski K, Wilmowicz E, Kućko A, Zienkiewicz A, Zienkiewicz K, Kopcewicz J. Molecular cloning of BLADE-ON PETIOLE gene and expression analyses during nodule development in Lupinus luteus. J Plant Physiol. 2015;179:35–39. https://doi.org/10.1016/j.jplph.2015.01.019

Frankowski K, Wilmowicz E, Kućko A, Zienkiewicz A, Zienkiewicz K, Kopcewicz J. Profiling the BLADE-ON-PETIOLE gene expression in the abscission zone of generative organs in Lupinus luteus. Acta Physiol Plant. 2015;37:220. https://doi.org/10.1007/s11738-015-1972-y

Kęsy J, Maciejewska B, Sowa M, Szumilak M, Kawałowski K, Borzuchowska M, et al. Ethylene and IAA interactions in the inhibition of photoperiodic flower induction of Pharbitis nil. Plant Growth Regul. 2008;55:43–50. https://doi.org/10.1007/s10725-008-9256-9

Yip WK, Dong JG, Kenny JW, Thompson GA, Yang SF. Characterization and sequencing of the active site of 1-aminocyclopropane-1-carboxylate synthase. Proc Natl Acad Sci USA 1990;87(20):7930–7934. https://doi.org/10.1073/pnas.87.20.7930

Huang PL, Parks JE, Rottmann WE, Theologis A. Two genes encoding 1-aminocyclopropane-1-carboxylate synthase in zucchini (Cucurbita pepo) are clustered and similar but differentially regulated. Proc Natl Acad Sci USA 1991;88(16):7021–7025. https://doi.org/10.1073/pnas.88.16.7021

Rottmann WH, Peter GF, Oeller PW, Keller JA, Shen NF, Nagy BP, et al. 1-Aminocyclopropane-1-carboxylate synthase in tomato is encoded by multigene family whose transcription is induced during fruit and floral senescence. J Mol Biol. 1991;222(4):937–961. https://doi.org/10.1016/0022-2836(91)90587-V

Yoo A, Seo YS, Jung JW, Sung SK, Kim WT, Lee W, et al. Lys296 and Arg299 residues in the C-terminus of MD-ACO1 are essential for a 1-aminocyclopropane-1-carboxylate oxidase enzyme activity. J Struct Biol. 2006;156(3):407–420. https://doi.org/10.1016/j.jsb.2006.08.012

Bleecker AB, Patterson SE. Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell. 1997;9(7):1169–1179. https://doi.org/10.1105/tpc.9.7.1169

Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, et al. INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell. 2003;15(10):2296–2307. https://doi.org/10.1105/tpc.014365

Pandita VK, Jindal KK. Enzymatic and anatomical changes in abscission zone cells of apple fruits induced by ethephon. Biol Plant. 1991;33(1):20–25. https://doi.org/10.1007/BF02873782

Gómez-Cadenas A, Mehouachi J, Tadeo FR, Primo-Millo E, Talon M. Hormonal regulation of fruitlet abscission induced by carbohydrate shortage in citrus. Planta. 2000;210(4):636–643. https://doi.org/10.1007/s004250050054

Clark DG, Richards C, Hilioti Z, Lind-Iversen S, Brown K. Effect of pollination on accumulation of ACC synthase and ACC oxidase transcripts, ethylene production and flower petal abscission in geranium (Pelargonium × hortorum L.H. Bailey). Plant Mol Biol. 1997;34(6):855–865. https://doi.org/10.1023/A:1005877809905

Tudela D, Primo-Millo E. 1-Aminocyclopropane-1-carboxylic acid transported from roots to shoots promotes leaf abscission in Cleopatra mandarin (Citrus reshni Hort. ex Tan.) seedlings rehydrated after water stress. Plant Physiol. 1992;100(1):131–137. https://doi.org/10.1104/pp.100.1.131

Roberts JA, Elliot KA, Gonzalez-Carranza ZH. Abscission, dehiscence and other cell separation processes. Ann Rev Plant Biol. 2002;53:131–158. https://doi.org/10.1146/annurev.arplant.53.092701.180236

Sexton R, Roberts JA. Cell biology of abscission. Ann Rev Plant Physiol. 1982;33:133–162. https://doi.org/10.1146/annurev.pp.33.060182.001025

Kende H. Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol. 1993;44:283–307. https://doi.org/10.1146/annurev.pp.44.060193.001435

Ralph SG, Hudgins JW, Jancsik S, Franceschi VR, Bohlmann J. Aminocyclopropane carboxylic acid synthase is a regulated step in ethylene-dependent induced conifer defense. Full-length cDNA cloning of a multigene family, differential constitutive, and wound- and insect-induced expression, and cellular and subcellular localization in spruce and Douglas fir. Plant Physiol. 2007;143(1):410–424. https://doi.org/10.1104/pp.106.089425

Takahashi H, Iwasa T, Shinkawa T, Kawahara A, Kurusu T, Inoue Y. Isolation and characterization of the ACC synthase genes from lettuce (Lactuca sativa L.), and the involvement in low pH-induced root hair initiation. Plant Cell Physiol. 2003;44(1):62–69. https://doi.org/10.1093/pcp/pcg008

Yamagami T, Tsuchisaka A, Yamada K, Haddon WF, Harden LA, Theologis A. Biochemical diversity among the 1-aminocyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J Biol Chem. 2003;278(49):49102–49112. https://doi.org/10.1074/jbc.M308297200

McCarthy DL, Capitani G, Feng L, Gruetter MG, Kirsch JF. Glutamate 47 in 1-aminocyclopropane-1-carboxylate synthase is a major specificity determinant. Biochemistry. 2001;40(41):12276–12284. https://doi.org/10.1021/bi011050z

Tatsuki M, Mori H. Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the C-terminal region. J Biol Chem. 2001;276(30):28051–28057. https://doi.org/10.1074/jbc.M101543200

Burdon JN, Sexton R. Ethylene co-ordinates petal abscission in red raspberry (Rubus idaeus L.) flowers. Ann Bot. 1993;72(4):289–294. https://doi.org/10.1006/anbo.1993.1110

Stead AD, Moore KG. Studies on flower longevity in Digitalis: pollination induced corolla abscission in Digitalis flowers. Planta. 1979;146(4):409–414. https://doi.org/10.1007/BF00380853

Israeli Y, Blumenfeld A. Ethylene production by banana flowers. HortScience. 1980;15:187–189.

Mayak S, Halevy AH, Katz M. Correlative changes in phytohormones in relation to senescence processes in rose petals. Physiol Plant. 1972;27(1):1–4. https://doi.org/10.1111/j.1399-3054.1972.tb01127.x

Wallner S, Kassalen R, Burgoon J, Craig R. Pollination, ethylene production and shattering in geraniums. HortScience. 1979;14:446.

Deneke CF, Evensen KB, Craig R. Regulation of petal abscission in Pelargonium × domesticum. HortScience. 1990;25(8):937–940.

Botton A, Eccher G, Forcato C, Ferrarini A, Begheldo M, Zermiani M, et al. Signaling path-ways mediating the induction of apple fruitlet abscission. Plant Physiol. 2011;155(1):185–208. https://doi.org/10.1104/pp.110.165779

Dal Cin V, Boschetti A, Dorigoni A, Ramina A. Benzylaminopurine appli-cation on two different apple cultivars (Malus domestica) displays new and unexpected fruitlet abscission features. Ann Bot. 2007;99(6):1195–1202. https://doi.org/10.1093/aob/mcm062

Nakano T, Fujisawa M, Shima Y, Ito Y. Expression profiling of tomato pre-abscission pedicels provides insights into abscission zone properties including competence to respond to abscission signals. BMC Plant Biol. 2013;13:40. https://doi.org/10.1186/1471-2229-13-40

Schnurr J, Shockey J, Browse J. The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell. 2004;16(3):629–642. https://doi.org/10.1105/tpc.017608

Jackson MB, Morrow IB, Osborne DJ. Abscission and dehiscence in the squirting cucumber, Ecballium elaterium: regulation by ethylene. Can J Bot. 1972;50(7):1465–1471. https://doi.org/10.1139/b72-179

Roberts JA, Schindler CB, Tucker GA. Ethylene-promoted tomato flower abscission and the possible involvement of an inhibitor. Planta. 1984;160(2):159–163. https://doi.org/10.1007/BF00392864