Abstract
Roots encounter cinnamic acid and its hydroxylated derivatives that are commonly found in soils. However, root systems consist of different root types with different morphological and physiological characteristics. Very little is known about the responses and adaptation mechanisms of the root types to cinnamic acid and its hydroxylated derivatives. In this study, the morphological and physiological responses of different maize root types exposed to different concentrations of t-cinnamic, ferulic, caffeic or p-coumaric acids were investigated. The results showed that the effects of allelochemicals were dependent on concentration, chemical structure, root type and process considered. In particular, t-cinnamic acid was characterized by higher allelopathic activity when compared with its derivatives, where a hydroxyl or methyl groups were present in aromatic ring. Among root types it was possible to delineate the following tolerance hierarchy: primary > seminal > nodal > lateral of the primary = lateral of the seminal roots. Moreover, primary and seminal roots showed a different strategy to cope the chemical stress by either increasing or decreasing specific root length. Finally, an electrophysiological approach identified an involvement of proton pump activity and consequently a decrease in nitrate uptake.
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Abenavoli MR, De Santis C, Sidari M, Sorgonà A, Badiani M, Cacco G (2001) Influence of coumarin on the net nitrate uptake in durum wheat. New Phytol 150:619–662
Abenavoli MR, Sorgonà A, Albano S, Cacco G (2004) Coumarin differentially affects the morphology of different root types of maize seedlings. J Chem Ecol 30:1871–1883
Abenavoli MR, Nicolò A, Lupini A, Oliva S, Sorgonà A (2008) Effects of different allelochemicals on root morphology of Arabidopsis thaliana. Allelopathy J 22:245–252
Abenavoli MR, Lupini A, Oliva S, Sorgonà A (2010) Allelochemical effects on net nitrate uptake and plasma membrane H+-ATPase activity in maize seedlings. Biol Plant 54:149–153
Aliotta G, Cafiero G, Fiorentino A, Strumia S (1993) Inhibition of radish germination and root growth by coumarin and phenylpropanoids. J Chem Ecol 19:175–183
Batish DR, Singh HP, Kaur S, Kohli RK, Yadav SS (2008) Caffeic acid affects early growth, and morphogenetic response of hypocotyl cuttings of mung bean (Phaseolus vulgaris). J Plant Physiol 165:297–305
Belz RG, Hurle K, Duke SO (2005) Dose–response—a challenge for allelopathy? Nonlinearity Biol Toxicol Med 3:173–211
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradient as common module for plant organ formation. Cell 115:591–602
Bergmark CL, Jackson WA, Volk RJ, Blum U (1992) Differential inhibition by ferulic acid of nitrate and ammonium uptake on Zea mays L. Plant Physiol 98:639–645
Blum U (1996) Allelopathic interactions involving phenolic acids. J Nematol 28:259–267
Blum U, Rebbeck J (1989) Inhibition and recovery of cucumber roots given multiple treatments of ferulic acid in nutrient culture. J Chem Ecol 15:917–928
Booker FL, Blum U, Fiscus EL (1992) Short-term effects of ferulic acid on ion uptake and water relations in cucumber seedlings. J Exp Bot 43:649–655
Bradford MM (1976) A rapid and sensitive method of quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254
Brault M, Amiar Z, Pennarun A-M, Monestiez M, Zhang Z, Cornel D, Dellis O, Knight H, Bouteau F, Rona J-P (2004) Plasma membrane depolarization induced by ABA in Arabidopsis thaliana suspension cells involves reduction of proton pumping in addition to anion channel activation which are both Ca2+ dependent. Plant Physiol 135:231–243
Bubna GA, Lima RB, Zanardo DYL, dos Santos WD, Ferrarese MLL, Ferrarese-Filho O (2011) Exogenous caffeic acid inhibits the growth and enhances the lignification of the roots of soybean (Glycine max). J Plant Physiol 168:1627–1633
Burgos NR, Talbert RE, Kim KS, Kuk YI (2004) Growth inhibition and root ultrastructure of cucumber seedlings exposed to allelochemicals from rye (Secale cereale). J Chem Ecol 30:671–689
Casimiro I, Beekman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171
Chou CH, Lin HJ (1976) Autointoxication mechanism of Oryza sativa I. Phytotoxic effects of decomposing rice residues in soil. J Chem Ecol 2:353–367
Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–868
De Smet I, Vanneste S, Inzé D, Beeckman T (2006) Lateral root initiation or the birth of a new meristem. Plant Mol Biol 60:871–887
Einhellig FA (1995) Mechanism of action of allelochemicals in allelopathy. In: Inderjit MM, Dakshini MM, Einhellig FA (eds) Allelopathy: organisms, processes, and applications. American Chemical Society, Washington, pp 96–116
Feix G, Hochholdinger F, Park WJ (2002) Maize root system and genetic analysis of its formation. In: Waisel Y, Eshel A, Kafka U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 239–248
Feldman L (1994) The maize root. In: Freeling M, Walbot V (eds) The maize handbook. Springer, New York, pp 29–37
Forbush B (1983) Assay of the Na+ K+-ATPase in plasma membrane preparations: increasing the permeability of membrane vesicles using sodium dodecyl sulfate buffered with bovine serum albumin. Anal Biochem 128:159–163
Giannini JL, Ruiz-Cristin J, Briskin DP (1988) A small scale procedure for the isolation of transport competent vesicles from plants tissues. Anal Biochem 174:561–567
Glass ADM, Dunlap J (1974) Influence of phenolic acids on ion uptake. IV. Depolarization of membrane potentials. Plant Physiol 54:855–858
Hartley RD, Whitehead DC (1985) Phenolic acids in soils and their influence on plant growth and soil microbial processes. In: Vaughan D, Malcom RE (eds) Developmnets in Plant and Soil sciences. Martinus Nijhoff, Dordrecht, pp 109–149
Hochholdinger F, Tuberosa R (2009) Genetics and genomics of root architecture in maize. Curr Opin Plant Biol 12:172–177
Hochholdinger F, Woll K, Sauer M, Demdinsky D (2004) Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann Bot 93:359–368
Holappa LD, Blum U (1991) Effects of exogenously applied ferulic acid, a potential allelopathic compound, on leaf growth, water utilization, and endogenous abscisic acid levels of tomato, cucumber, and bean. J Chem Ecol 17:865–886
Jankay P, Muller WH (1976) The relationships among umbelliferone, growth, and peroxidase levels in cucumber roots. Am J Bot 63:126–132
Jeschke WD, Holobrada M, Hartung W (1997) Growth of Zea mays L. plants with their seminal roots only. Effects on plant development, xylem transport, mineral nutrition and the flow and distribution of abscisic acid (ABA) as a possible shoot to root signal. J Exp Bot 48:1229–1239
Jitãreanu A, Boz I, Tãtãrîngã G, Zbancioc A, Stãnescu U (2013) The effects of some cinnamic acids derivatives on the architecture of Phaseolus vulgaris roots. Rom Biotechnol Lett 18:8317–8326
Kong X, Zhang M, De Smet I, Ding Z (2014) Designer crops: optimal root system architecture for nutrient acquisition. Trends Biotechnol 32:597–598
Kupidlowska E, Kowalec M, Sulkowski G, Zobel AM (1994) The effect of coumarin on root elongation and ultrastructure of meristematic cell protoplast. Ann Bot 73:525–530
Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R (2006) Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 47:788–792
Lupini A, Sorgonà A, Miller AJ, Abenavoli MR (2010) Short-time effects of coumarin along the maize primary root axis. Plant Signal Behav 5:1395–1400
Lupini A, Araniti F, Sunseri F, Abenavoli MR (2014) Coumarin interacts with auxin polar transport to modify root system architecture in Arabidopsis thaliana. Plant Growth Regul 74:23–31
Luxovà M, Kozinka V (1970) Structure and conductivity of the corn root system. Biol Plant 12:47–57
Lyu SW, Blum U (1990) Effects of ferulic acid, an allelopathic compound, on net P, K, and water uptake by cucumber seedlings in a split-root system. J Chem Ecol 16:2429–2439
Macías FA (1995) Allelopathy in the search for natural herbicides models. In: Inderjit, Darkshini KMM, Einhellig FA (eds) Allelopathy: organisms, processes and applications, ACS symposium series 582. American Chemical Society, Washington, pp 310–329
Maffei ME, Mithöfer A, Boland W (2007) Before gene expression: early events in plant–insect interaction. Trends Plant Sci 12:310–316
McCully ME (1999) Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Biol 50:695–718
Miller AJ, Smith SJ (1996) Nitrate transport and compartmentation in cereal root cells. J Exp Bot 47:843–854
Miller AJ, Cookson SJ, Smith SJ, Wells DM (2001) The use of microelectrodes to investigate compartmentation and the transport of metabolized inorganic ions in plants. J Exp Bot 52:541–549
Moloney MM, Elliott MC, Cleland RE (1981) Acid growth effects in maize roots: evidence for a link between auxin-economy and proton extrusion in the control of root growth. Planta 152:285–291
Morsomme P, Boutry M (2000) The plant plasma-membrane H+-ATPase: structure, function and regulation. Biochim Biophys Acta 1465:1–16
Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29
Pramanik MHR, Nagal M, Asao M, Matsui Y (2000) Effect of temperature and photoperiod on phytotoxic root exudates of cucumber (Cucumis sativus) in hydroponic culture. J Chem Ecol 26:1953–1967
Rayle D, Cleland DE (1970) Enhancement of wall loosening and elongation by acid solutions. Plant Physiol 46:250–253
Romano A, Sorgonà A, Lupini A, Araniti F, Stevanato P, Cacco G, Abenavoli MR (2013) Morpho-physiological responses of sugar beet (Beta vulgaris L.) genotypes to drought stress. Acta Physiol Plant 35:853–865
Ryser P (2006) The mysterious root length. Plant Soil 286:1–6
Santi S, Locci G, Pinton R, Cesco S, Varanini Z (1995) Plasma membrane H+-ATPase in maize roots induced for NO3 − uptake. Plant Physiol 109:1277–1283
Schubert S, Schubert E, Mengel K (1990) Effect of low pH of the root medium on proton release, growth, and nutrient uptake of field beans (Vicia faba). Plant Soil 124:239–244
Sorgonà A, Lupini A, Mercati F, Di Dio L, Sunseri F, Abenavoli MR (2011) Nitrate uptake along the maize primary root: an integrated physiological and molecular approach. Plant Cell Environ 34:1127–1140
Svensson SB (1971) The effect of coumarin on root growth and root histology. Physiol Plant 24:446–470
Sze H (1985) H+-translocating ATPases: advances using membrane vesicles. Annu Rev Plant Physiol 36:113–122
Varney GT, McCully ME (1991) The branch roots of Zea. II. Developmental loss of the apical meristem in field-grown roots. New Phytol 118:535–546
Vaughan D, Ord BG (1991) Extraction of potential allelochemicals and their effects on root morphology and nutrient contents. In: Atkinson D (ed) Plant root growth. An ecological perspective. Blackwell Scientific, Oxford, pp 399–421
Waisel Y, Eshel A (2002) Functional diversity of various constituents of a single root system. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 157–174
Wang XL, Canny MJ, McCully ME (1991) The water status of the roots of soil-grown maize in relation to the maturity of their xylem. Physiol Plant 82:157–162
Wang XL, McCully ME, Canny MJ (1995) The branch roots of Zea V. Structural features that may influence water and nutrient uptake. Bot Acta 108:209–219
Whitehead DC (1964) Identification of p-hydroxybenzoic, vanillic, p-coumaric and ferulic acids in soils. Nature 202:417–418
Wong WS, Guo D, Wang XL, Yin ZQ, Xia B, Li N (2005) Study of cis-cinnamic acid in Arabidopsis thaliana. Plant Physiol Biochem 43:929–937
Xu L, Niu J, Li C, Zhang F (2009) Growth, nitrogen uptake and flow in maize plants affected by root growth restriction. J Integr Plant Biol 51:689–697
Yan F, Schubert S, Mengel K (1992) Effect of low root medium pH on net proton release, root respiration, and growth of corn (Zea mays L.) and broad bean (Vicia faba L.). Plant Physiol 99:415–421
Yan H, Li K, Ding H, Liao C, Li X, Yuan L, Li C (2011) Root morphological and proteomic responses to growth restriction in maize plants supplied with sufficient N. J Plant Physiol 168:1067–1075
Yu JQ, Matsui Y (1997) Effects of root exudates of cucumber (Cucumis sativus) and allelochemicals on ion uptake by cucumber seedlings. J Chem Ecol 23:817–827
Yu P, Li X, Yuan L, Li C (2014) A novel morphological response of maize (Zea mays) adult roots to heterogeneous nitrate supply revealed by a split-root experiment. Physiol Plant 150:133–144
Zanardo DIL, Lima RB, Ferrarese MLL, Bubna GA, Ferrarese-Filho O (2009) Soybean root growth inhibition and lignification induced by p-coumaric acid. Environ Exp Bot 66:25–30
Zažímalová E, Murphy AS, Yang H, Hoyerová K, Hosek P (2010) Auxin transporters: why so many? Cold Spring Harb Perspect Biol 2:a001552
Zobel RW (1995) Genetic and environmental aspects of roots and seedlings stress. Hort Sci 30:1189–1192
Zobel AM, Brown SA (1995) Coumarins in the interaction between the plant and its environment. Allelopathy J 2:9–22
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Supplemental Fig. 1
Compounds used in this study. A, t-cinnamic acid; B, p-coumaric acid; C, caffeic acid; D, ferulic acid (JPEG 27 kb)
Supplemental Fig. 2
Representative pictures of maize seedlings exposed to 300 μM allelochemicals for 24 h (A, control; B, t-cinnamic acid; C, caffeic acid; D, ferulic acid; E, p-coumaric acid) (JPEG 39 kb)
Supplemental Fig. 3
Nodal roots exposed to the allelochemicals, p-coumaric (PC); ferulic (FER), caffeic (CAF), t-cinnamic (CIN), acids for 48 h. The values are showed as mean ± SE (n = 7). * = significant different at p < 0.05 respect to control (line), according to Student’s unpaired t test (JPEG 713 kb)
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Lupini, A., Sorgonà, A., Princi, M.P. et al. Morphological and physiological effects of trans-cinnamic acid and its hydroxylated derivatives on maize root types. Plant Growth Regul 78, 263–273 (2016). https://doi.org/10.1007/s10725-015-0091-5
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DOI: https://doi.org/10.1007/s10725-015-0091-5