Dehydrocostus lactone, a naturally occurring polar auxin transport inhibitor, inhibits epicotyl growth by interacting with auxin in etiolated Pisum sativum seedlings

Yuta Toda, Kazuho Okada, Junichi Ueda, Kensuke Miyamoto

Abstract


We have isolated germacranolide-type sesquiterpene lactones with an α-methylene-γ-lactone moiety, dehydrocostus lactone (DHCL), costunolide, santamarine, and a novel compound denoted artabolide [3-hydroxy-4,6,7(H)-germacra-1(10),11(13)-dien-6,12-olide] from oriental medicinal Asteraceae plants as novel naturally occurring inhibitors of polar auxin transport detected by the radish hypocotyl bioassay. To investigate the mode of action of natural sesquiterpene lactones on the inhibition of polar auxin transport as well as its relation to the growth of seedlings, the function of DHCL on growth and auxin dynamics in etiolated pea seedlings was studied intensively. DHCL reduced polar auxin transport in a dose-dependent manner together with the inhibition of the accumulation of mRNA of PsAUX1 and PsPIN1 genes encoding influx and efflux carrier proteins of auxin, respectively. DHCL applied to the apical hook region as a lanolin paste substantially inhibited elongation growth in the subapical region of epicotyls in intact etiolated pea seedlings, coupled with a significant reduction of endogenous levels of indole-3-acetic acid (IAA). DHCL also revealed the inhibition of IAA-induced cell elongation in etiolated pea epicotyl segments by affecting IAA-induced changes in the mechanical properties of cell walls. These facts suggest that germacranolide-type sesquiterpene lactones with an α-methylene-γ-lactone moiety affect the expression of PsAUX1 and PsPINs genes, and then inhibit polar auxin transport and reduce endogenous levels of IAA necessary for stem growth in etiolated pea seedlings. These compounds are also suggested to show the inhibitory effects on auxin action in pea stem growth.

Keywords


auxin; cell wall mechanical properties; endogenous IAA level; IAA-induced elongation; inhibitor; pea epicotyls; polar auxin transport

Full Text:

PDF

References


Muday GK, Murphy AS. An emerging model of auxin transport regulation. Plant Cell. 2002;14:293–299. https://doi.org/10.1105/tpc.140230

Scarpella E, Marcos D, Friml J, Berleth T. Control of leaf vascular patterning by polar auxin transport. Genes Dev. 2006;20:1015–1027. https://doi.org/10.1101/gad.1402406

Adamowski M, Friml J. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell. 2015;27:20–32. https://doi.org/10.1105/tpc.114.134874

Ueda J, Saniewski M, Miyamoto K. Auxins, one major plant hormone, in soil. In: Szajdak LW, editor. Bioactive compounds in agricultural soils. Cham: Springer; 2016. p. 175–206. https://doi.org/10.1007/978-3-319-43107-9

Jensen PJ, Hangarter RP, Estelle M. Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol. 1998;116:455–462. https://doi.org/10.1104/pp.116.2.455

Keuskamp DH, Pollmann S, Voesenek LACJ, Peerers AJM, Pierik R. Auxin transport through PIN-FORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc Natl Acad Sci USA. 2010;107:22740–22744. https://doi.org/10.1073/pnas.1013457108

Chaiwanon J, Wang W, Zhu JY, Oh E, Wang ZY. Information integration and communication in plant growth regulation. Cell. 2016;164:1257–1268. https://doi.org/10.1016/j.cell.2016.01.044

Ueda J, Sakamoto-Kanetake M, Toda Y, Miyamoto K, Uheda E, Daimon H. Auxin polar transport is essential for the early growth stage of etiolated maize (Zea mays L. cv. Honey Bantam) seedlings. Plant Prod Sci. 2014;17:144–151. https://doi.org/10.1626/pps.17.144

Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell. 1991;3:677–684. https://doi.org/10.1105/tpc.3.7.677

Oka M, Miyamoto K, Okada K, Ueda J. Auxin polar transport and flower formation in Arabidopsis thaliana transformed with indoleacetamide hydrolase (iaaH) gene. Plant Cell Physiol. 1999;40:231–237. https://doi.org/10.1093/oxfordjournals.pcp.a029532

Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science. 1998;282:2226–2230. https://doi.org/10.1126/science.282.5397.2226

Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, et al. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 1999;18:2066–2073. https://doi.org/10.1093/emboj/18.8.2066

Křeček P, Skůpa P, Libus J, Naramoto S, Tejos R, Friml J, et al. The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol. 2009;10:249. https://doi.org/10.1186/gb-2009-10-12-249

Luschnig C, Vert G. The dynamics of plant membrane proteins: PINs and beyond. Development. 2014;141:2924–2936. https://doi.org/10.1242/dev.103424

Klíma P, Laňková M, Zažímalová E. Inhibitors of plant hormone transport. Protoplasma. 2016;253:1391–1404. https://doi.org/10.1007/s00709-015-0897-z

Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hasek J, et al. Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Natl Acad Sci USA. 2008;105(11):4489–4494. https://doi.org/10.1073/pnas.0711414105

Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature. 2001;413:425–428. https://doi.org/10.1038/35096571

Kojo KH, Yasuhara H, Hasezawa S. Time-sequential observation of spindle and phragmoplast orientation in BY-2 cells with altered cortical actin microfilament patterning. Plant Signal Behav. 2014;9(8):e29579. https://doi.org/10.4161/psb.29579

Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, et al. Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol. 2001;126:524–535. https://doi.org/10.1104/pp.126.2.524

Rahman A, Ahamed A, Amakawa T, Goto N, Tsurumi S. Chromosaponin I specifically interacts with AUX1 protein in regulating the gravitropic response of Arabidopsis roots. Plant Physiol. 2001;125:990–1000. https://doi.org/10.1104/pp.125.2.990

Steenackers W, Cesarino I, Klíma P, Quareshy M, Vanholme R, Corneillie S, et al. The allelochemical MDCA inhibits lignification and affects auxin homeostasis. Plant Physiol. 2016;172:874–888. https://doi.org/10.1104/pp.15.01972

Steenackers W, Klíma P, Quareshy M, Cesarino I, Kumpf RP, Corneillie S, et al. cis-Cinnamic acid is a novel, natural auxin efflux inhibitor that promotes lateral root formation. Plant Physiol. 2017;173:552–565. https://doi.org/10.1104/pp.16.00943

Ueda J, Toda Y, Kato K, Kuroda Y, Arai T, Hasegawa T, et al. Identification of dehydrocostus lactone and 4-hydroxy-β-thujone as auxin polar transport inhibitors. Acta Physiol Plant. 2013;35:2251–2258. https://doi.org/10.1007/s11738-013-1261-6

Toda Y, Shigemori H, Ueda J, Miyamoto K. Isolation and identification of auxin polar transport inhibitors from Saussurea costus and Atractylodes japonica. Acta Agrobot. 2017;70(3):1700. https://doi.org/10.5586/aa.1700

Arai T, Toda Y, Kato T, Miyamoto K, Hasegawa T, Yamada K, et al. Artabolide, a novel polar auxin transport inhibitor isolated from Artemisia absinthium. Tetrahedron. 2013;69:7001–7005. https://doi.org/10.1016/j.tet.2013.06.052

Panda CK, Choudhury K, Sanyal U, Chakraborti SK. Mechanism of action of alpha-methylene-gamma-lactone derivatives of substituted nucleic acid bases in tumor cells. Chemotherapy. 1989;35:174–180. https://doi.org/10.1159/000238667

Kretschmer N, Rinner B, Stuendl N, Kaltengger H, Wolf E, Kunert O, et al. Effect of costunolide and dehydrocostus lactone on cell cycle, apoptosis, and ABC transporter expression in human soft tissue sarcoma cells. Planta Med. 2012;78:1749–1756. https://doi.org/10.1055/s-0032-1315385

Kumar A, Kumar S, Kumar D, Agnihotri VK. UPLC/MS/MS method for quantification and cytotoxic activity of sesquiterpene lactones isolated from Saussurea lappa. J Ethnopharmacol. 2014;155:1393–1397. https://doi.org/10.1016/j.jep.2014.07.037

Gach K, Janecka A. α-Methylene-γ-lactones as a novel class of anti-leukemic agents. Anticancer Agents Med Chem. 2014;14:688–694. https://doi.org/10.2174/1871520614666140313095010

Sun X, Kang H, Yao Y, Chen H, Sun L, An W, et al. Dehydrocostus lactone suppressed the proliferation, migration, and invasion of colorectal carcinoma through the downregulation of eIF4E expression. Anticancer Drugs. 2015;26:641–648. https://doi.org/10.1097/CAD.0000000000000229

Tabata K, Nishimura Y, Takeda T, Kurita M, Uchiyama T, Suzuki T. Sesquiterpene lactones derived from Saussurea lappa induce apoptosis and inhibit invasion and migration inn neuroblastoma cells. J Pharmacol Sci. 2015;127:397–403. https://doi.org/10.1016/j.jphs.2015.01.002

Chen LG, Jan YS, Tsai PW, Norimoto H, Michihara S, Murayama C. Anti-inflammatory and antinociceptive constituents of Atractylodes japonica Koizumi. J Agric Food Chem. 2016;64:2254–2262. https://doi.org/10.1021/acs.jafc.5b05841

Joel DM, Chaudhuri SK, Plakhine D, Ziadna H, Steffens JC. Dehydrocostus lactone is exuded from sunflower roots and stimulates germination of the root parasite Orobanche cumana. Phytochemistry. 2011;72:624–634. https://doi.org/10.1016/j.phytochem.2011.01.037

Raupp FM, Spring O. New sesquiterpene lactones from sunflower root exudate as germination stimulator for Orobanche cumana. J Agric Food Chem. 2013;61(44):10481–10487. https://doi.org/10.1021/jf402392e

Ueno K, Furumoto T, Umeda S, Mizutani M, Takikawa H, Batchvarova R, et al. Heliolacton, a non-sesquiterpene lactone germination stimulant for root parasitic weed from sunflower. Phytochemistry. 2014;108:122–128. https://doi.org/10.1016/j.phytochem.2014.09.018

Miyamoto K, Kamisaka S. Stimulation of Pisum sativum epicotyl elongation by gibberellin and auxin – different effects of two hormones on osmoregulation and cell walls. Physiol Plant. 1988;74:457–466. https://doi.org/10.1111/j.1399-3054.1988.tb02003.x

Hoshino T, Hitotsubashi R, Miyamoto K, Tanimoto E, Ueda J. Isolation of PsPIN2 and PsAUX1 from etiolated pea epicotyls and their expression on a three-dimensional clinostat. Adv Space Res. 2005;36:1284–1291. https://doi.org/10.1016/j.asr.2005.03.121

Hoshino T, Miyamoto K, Ueda J. Gravity-controlled asymmetrical transport of auxin regulates a gravitropic response in the early growth stage of etiolated pea (Pisum sativum) epicotyls: studies using simulated microgravity conditions on a three-dimensional clinostat and using an agravitropic mutant, ageotropum. J Plant Res. 2007;120:619–628. https://doi.org/10.1007/s10265-007-0103-2

Ueda J, Tada T, Hoshino T, Miyamoto K, Uheda E, Oka M. Isolation of PsPINs and PsAUX1 cDNA encoding putative auxin efflux and influx carriers and/or facilitators, respectively from etiolated epicotyls of an agavitropic pea (Pisum sativum L.) mutant, ageotropum. Biol Sci Space. 2012;26:32–41. https://doi.org/10.2187/bss.26.32

Yokota T, Murofushi N, Takahashi N. Extraction, purification, and identification. In: MacMillan J, editor. Hormonal regulation of development I. Berlin: Springer; 1980. p. 113–201. (Encyclopedia of Plant Physiology; vol 9). https://doi.org/10.1007/978-3-642-67704-5_3

Tanimoto E, Fujii S, Yamamoto R, Inanaga S. Measurement of viscoelastic properties of root cell walls affected by low pH in lateral roots of Pisum sativum L. Plant Soil. 2000;226:21–28. https://doi.org/10.1023/A:1026460308158

Hu W, Fagundez S, Katin-Gazzini L, Li Y, Li W, Chen Y, et al. Endogenous auxin and its manipulation influence in vitro shoot organogenesis of citrus epicotyl explants. Hortic Res. 2017;4:17071. https://doi.org/10.1038/hortres.2017.71

Miyamoto K, Uheda E, Oka M, Ueda J. Auxin polar transport and automorphosis in plants. Biol Sci Space. 2011;25:57–68. https://doi.org/10.2187/bss.25.57

Petrášek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science. 2006;312:914–918. https://doi.org/10.1126/science.1123542

Wiśniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, et al. Polar PIN localization directs auxin flow in plants. Science. 2006;312:883. https://doi.org/10.1126/science.1121356

Chawla R, DeMason DA. Molecular expression of PsPIN1, a putative auxin efflux carrier gene from pea (Pisum sativum L.). Plant Growth Regul. 2004;44:1–14. https://doi.org/10.1007/s10725-004-2139-9

Chen R, Masson PH. Auxin transport and recycling of PIN proteins in plants. In: Šamaja J, Balška F, Menzel D, editors. Plant endocytosis. Berlin: Springer; 2005. p. 139–157. https://doi.org/10.1007/7089_009

Kamada M, Miyamoto K, Oka M, Ueda J, Higashibata A. Regulation of asymmetric polar auxin transport by PsPIN1 in endodermal tissues of etiolated Pisum sativum epicotyls: focus on immunohistochemical analyses. J Plant Res. 2018;134:681–692. https://doi.org/10.1007/s10265-018-1031-z

Muday GK, Brunn SA, Haworth P, Subramanian M. Evidence for a single naphthylphthalamic acid binding site on the zucchini plasma membrane. Plant Physiol. 1993;103:449–456. https://doi.org/10.1104/pp.103.2.449

Sussman MR, Goldsmith MHM. The action of specific inhibitors of auxin transport on uptake and binding of N-1-naphthylphtalamic acid to a membrane site in maize coleoptiles. Planta. 1981;152:13–18. https://doi.org/10.1007/BF00384978

Sorce C, Picciarelli P, Calistri G, Lercari B, Ceccarelli N. The involvement of indole-3-acetic acid in the control of stem elongation in dark- and light-grown pea (Pisum sativum) seedlings. J Plant Physiol. 2008;165:482–489. https://doi.org/10.1016/j.jphl.2007.03.012

Zhao GW, Wang JH. Effect of auxin on mesocotyl elongation of dark-grown maize under different seedling depth. Russ J Plant Physiol. 2010;57:79–86. https://doi.org/10.1134/S1021443710010115

Bandurski RS, Schulze A, Cohen JD. Photoregulation of the ratio of ester to free indole-3-acetic acid. Biochem Biophys Res Commun. 1977;79:1219–1223. https://doi.org/10.1016/0006-291X(77)91136-6

Goldsmith MHM. The polar transport of auxin. Annu Rev Plant Physiol. 1977;28:439–478. https://doi.org/10.1146/annurev.pp.28.060177.002255

Wakabayashi K, Sakurai N, Kuraishi S. Effect of ABA on synthesis of cell-wall polysaccharides in segments of etiolated squash hypocotyl. II. Levels of UDP-neutral sugars. Plant Cell Physiol. 1991;32:427–432. https://doi.org/10.1093/oxfordjournals.pcp.a078097

Ueda J, Miyamoto K, Aoki M. Jasmonic acid inhibits the IAA-induced elongation of oat coleoptile segments: a possible mechanism involving the metabolism of cell wall polysaccharides. Plant Cell Physiol. 1994;35:1065–1070. https://doi.org/10.1093/oxfordjournals.pcp.a078695

Tanimoto E, Homma T, Matsuo K, Hoshino T, Lux A, Luxová, M. Root structure and cell wall extensibility of adventitious roots of tea (Camellia sinensis cv. Yabukita). Biologia. 2004;59(13 suppl):57–66.

Tanimoto E. Regulation of root growth by plant hormones – roles for auxin and gibberellin. Crit Rev Plant Sci. 2005;24:249–265. https://doi.org/10.1080/07352680500196108

Carpita NC. Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Biol. 1996;53:421–447. https://doi.org/10.1146/annurev.arplant.47.1.445

Nishitani K, Tominaga R. Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem. 1992;267:21058–21064.

Cosgrove DJ. Enzymes and other agents that enhance cell wall extensibility. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:391–417. https://doi.org/10.1146/annurev.arplant.50.1.391

Inouhe M, Yamamoto R, Masuda Y. Inhibition of IAA-induced cell elongation in Avena coleoptile segments by galactose: its effect on UDP-glucose formation. Physiol Plant. 1986;66:370–376. https://doi.org/10.1111/j.1399-3054.1986.tb05937.x

Inouhe M, Yamamoto R, Masuda Y. UDP-glucose level as a limiting factor for IAA-induced cell elongation in Avena coleoptile segments. Physiol Plant. 1987;69:49–54. https://doi.org/10.1111/j.1399-3054.1987.tb01944.x