Abstract
Duckweeds, quick-growing aquatic plants, have been recently recognized as promising hosts for the large-scale production of recombinant proteins and as an ideal biomass feedstock for biofuel production. These possible wide-spread industrial uses of duckweeds intensified research aimed at understanding the mechanisms that control duckweed growth. Here, we describe how the hormone cytokinin affects growth. We performed a number of standard cytokinin growth- and physiological-response assays using sterile-grown colonies of Lemna gibba and Spirodela polyrhiza. Similar to land plants, cytokinin inhibited root elongation in duckweeds. Surprisingly, and in contrast to land plants, cytokinin promoted growth of aerial organs in both duckweed species, suggesting that the cytokinin growth response fundamentally differs between aquatic and land plants.
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References
Appenroth KJ, Crawford DJ, Les DH (2015) After the genome sequencing of duckweed—how to proceed with research on the fastest growing angiosperm? Plant Biol 17:1–4. https://doi.org/10.1111/plb.12248
Cary AJ, Liu W, Howell SH (1995) Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol 107:1075–1082
Catarecha P et al (2007) A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133. https://doi.org/10.1105/tpc.106.041871
Chaloupkova K, Smart CC (1994) The abscisic acid induction of a novel peroxidase is antagonized by cytokinin in Spirodela polyrrhiza L. Plant Physiol 105:497–507
Cortleven A, Schmülling T (2015) Regulation of chloroplast development and function by cytokinin. J Exp Bot 66:4999–5013. https://doi.org/10.1093/jxb/erv132
Cui W, Cheng JJ (2015) Growing duckweed for biofuel production: a review. Plant Biol 17:16–23. https://doi.org/10.1111/plb.12216
Deikman J, Hammer P (1995) Induction of anthocyanin accumulation by cytokinins in Arabidopsis thaliana. Plant Physiol 108:47–57
Higuchi M et al (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101:8821–8826. https://doi.org/10.1073/pnas.04028871010402887101
Horiguchi G, Ferjani A, Fujikura U, Tsukaya H (2006) Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana. J Plant Res 119:37–42. https://doi.org/10.1007/s10265-005-0232-4
Hutchison CE et al (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–3087. https://doi.org/10.1105/tpc.106.045674
Imamura T, Sekine KT, Yamashita T, Kusano H, Shimada H (2016) Production of recombinant thanatin in watery rice seeds that lack an accumulation of storage starch and proteins. J Biotechnol 219:28–33. https://doi.org/10.1016/j.jbiotec.2015.12.006
Körner S, Vermaat JE, Veenstra S (2003) The capacity of duckweed to treat wastewater: ecological considerations for a sound design. J Environ Qual 32:1583–1590
Kubasek WL, Shirley BW, McKillop A, Goodman HM, Briggs W, Ausubel FM (1992) Regulation of flavonoid biosynthetic genes in germinating Arabidopsis seedlings. Plant Cell 4:1229–1236. https://doi.org/10.1105/tpc.4.10.12294/10/1229
Landolt E, Kandeler R (1987) The family of Lemnaceae—a monographic study: phytochemistry, physiology, application, bibliography, vol 2. Geobotanical Institute of the ETH, Zurich
Leão GA, de Oliveira AA, Felipe RTA, Santos Farnese F, Soares Gusman G (2013) Anthocyanins, thiols, and antioxidant scavenging enzymes are involved in Lemna gibba tolerance to arsenic. J Plant Interact 9:143–151. https://doi.org/10.1080/17429145.2013.784815
Les DH, Landolt E, Crawford DJ (1997) Systematics of the Lemnaceae (duckweeds): inferences from micromolecular and morphological data. Plant Syst Evol 204:161–177
Letham DS (1967) Regulators of cell division in plant tissues: V. A comparison of the activities of zeatin and other cytokinins in five bioassays. Planta 74:228–242. https://doi.org/10.1007/BF00384844
Li Y, Van den Ende W, Rolland F (2014) Sucrose induction of anthocyanin biosynthesis is mediated by DELLA. Mol Plant 7:570–572. https://doi.org/10.1093/mp/sst161
Liu Q, Zhu Y, Tao H, Wang N, Wang Y (2006) Damage of PS II during senescence of Spirodela polyrrhiza explants under long-day conditions and its prevention by 6-benzyladenine. J Plant Res 119:145–152. https://doi.org/10.1007/s10265-006-0259-1
McClure JW, Alston RE (1966) A chemotaxonomic study of Lemnaceae. Amer J Bot 53:849–860
McCombs PJ, Ralph RK (1972a) Cytokinin control of growth of Spirodela oligorrhiza in darkness. Planta 107:97–109. https://doi.org/10.1007/BF00387716
McCombs PJ, Ralph RK (1972b) Protein, nucleic acid and starch metabolism in the duckweed, Spirodela oligorrhiza, treated with cytokinins. Biochem J 129:403–417
Miyazawa Y, Sakai A, Miyagishima S, Takano H, Kawano S, Kuroiwa T (1999) Auxin and cytokinin have opposite effects on amyloplast development and the expression of starch synthesis genes in cultured bright yellow-2 tobacco cells. Plant Physiol 121:461–469
Miyazawa Y, Kato H, Muranaka T, Yoshida S (2002) Amyloplast formation in cultured tobacco BY-2 cells requires a high cytokinin content. Plant Cell Physiol 43:1534–1541
Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol 52:89–118
Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377
Stomp AM (2005) The duckweeds: a valuable plant for biomanufacturing. Biotechnol Annu Rev 11:69–99. https://doi.org/10.1016/S1387-2656(05)11002-3
Stoynova-Bakalova E, Karanov E, Petrov P, Hall MA (2004) Cell division and cell expansion in cotyledons of Arabidopsis seedlings. New Phytol 162:471–479
Thorsteinsson B, Eliasson L (1990) Growth retardation induced by nutritional deficiency or abscisic acid in Lemna gibba: The relationship between growth rate and endogenous cytokinin content. Plant Growth Regul 9:171–181
To JP, Kieber JJ (2008) Cytokinin signaling: two-components and more. Trends Plant Sci 13:85–92. https://doi.org/10.1016/j.tplants.2007.11.005
To J et al (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16:658–671. https://doi.org/10.1105/tpc.018978
Tsukaya H, Ohshima T, Naito S, Chino M, Komeda Y (1991) Sugar-dependent expression of the CHS-A gene for chalcone synthase from petunia in trangenic Arabidopsis. Plant Physiol 97:1414–1421
Utami D, Kawahata A, Sugawara M, Jog RN, Miwa K, Morikawa M (2018) Effect of exogenous general plant growth regulators on the growth of the duckweed Lemna minor. Front Chem 6:251. https://doi.org/10.3389/fchem.2018.00251
Veen J (1975) Preliminary studies of the flavonid patters of Lemna gibba L. and Lemna minor L. Aquat Bot 1:417–421
Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538. https://doi.org/10.1016/j.pbi.2009.07.002
Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492. https://doi.org/10.1073/pnas.171304098
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 15:2532–2550
Werner T et al (2008) Cytokinin deficiency causes distinct changes of sink and source parameters in tobacco shoots and roots. J Exp Bot 59:2659–2672. https://doi.org/10.1093/jxb/ern134
Werner T, Nehnevajova E, Kollmer I, Novak O, Strnad M, Kramer U, Schmülling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920. https://doi.org/10.1105/tpc.109.072694
Winkel BSJ (2006) The biosynthesis of flavonoids. In: Grotewold E (ed) The science of flavonoids. Springer, New York, pp 71–96
Acknowledgements
We thank Rutgers Duckweed Stock Cooperative for the duckweed species and Drs. S. DeBolt and M. Nair for help with the confocal microsopy. This work was supported by the USDA National Institute of Food and Agriculture, HATCH Project 1009329, and by the Kentucky Tobacco Research and Development Center. Confocal microscopy work was supported by the National Science Foundation under Cooperative Agreement No. 1355438.
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Kurepa, J., Shull, T.E. & Smalle, J.A. Cytokinin-induced growth in the duckweeds Lemna gibba and Spirodela polyrhiza. Plant Growth Regul 86, 477–486 (2018). https://doi.org/10.1007/s10725-018-0446-9
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DOI: https://doi.org/10.1007/s10725-018-0446-9