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Tree Fern Cyathea Lepifera May Survive by Its Phytotoxic Property

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Tree Fern Cyathea Lepifera May Survive by Its Phytotoxic Property plants Article Tree Fern Cyathea lepifera May Survive by Its Phytotoxic Property 1, , 2 3 2 Noriyuki Ida * y, Arihiro Iwasaki , Toshiaki Teruya , Kiyotake Suenaga and Hisashi Kato-Noguchi 1 1 Department of Applied Biological Science, Faculty of Agriculture, Kagawa University, Miki, Kagawa 761-0795, Japan; [email protected] 2 Department of Chemistry, Faculty of Science and Technology, Keio University, 3-14-1 Hiyoshi, Kohoku, Yokohama 223-8522, Japan; [email protected] (A.I.); [email protected] (K.S.) 3 Faculty of Education, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan; [email protected] * Correspondence: [email protected]; Tel.: +81-29-840-3211 Present address: Maruwa Biochemical Co., Ltd., Oaza-hoshinosato, Ami-machi, Inashiki-Gun, y Ibaraki 300-0326, Japan. Received: 10 December 2019; Accepted: 27 December 2019; Published: 28 December 2019 Abstract: Cyatheaceae (tree ferns) appeared during the Jurassic period and some of the species still remain. Those species may have some morphological and/or physiological characteristics for survival. A tree fern was observed to suppress the growth of other ligneous plants in a tropical forest. It was assumed that the fern may release toxic substances into the forest floor, but those toxic substances have not yet been identified. Therefore, we investigated the phytotoxicity and phytotoxic substances of Cyathea lepifera (J. Sm. ex Hook.) Copel. An aqueous methanol extract of C. lepifera fronds inhibited the growth of roots and shoots of dicotyledonous garden cress (Lepidum sativum L.), lettuce (Lactuca sativa L.), and alfalfa (Medicago sativa L.), and monocotyledonous ryegrass (Lolium multiflorum Lam.), timothy (Phleum pratense L.), and barnyardgrass (Echinochloa crus-galli (L.) P. Beauv.). The results suggest that C. lepifera fronds may have phytotoxicity and contain some phytotoxic substances. The extract was purified through several chromatographic steps during which inhibitory activity was monitored, and p-coumaric acid and (-)-3-hydroxy-β-ionone were isolated. Those compounds showed phytotoxic activity and may contribute to the phytotoxic effects caused by the C. lepifera fronds. The fronds fall and accumulate on the forest floor through defoliation, and the compounds may be released into the forest soils through the decomposition process of the fronds. The phytotoxic activities of the compounds may be partly responsible for the fern’s survival. Keywords: Cyathea lepifera; tree fern; growth inhibitor; phytotoxicity 1. Introduction Cyatheaceae, a tree fern family, is distributed in tropical and subtropical forests. The tree ferns grow to 20 m high and have very large fronds reaching 3–4 m in length. Cyatheaceae appeared during the Jurassic period and are considered living fossils. Most species are extinct, but some have survived [1]. Those surviving species may have special morphological and/or physiological traits for survival. The spatial occupation of Cyathea muricata (Cyatheaceae) in tropical forests was investigated in Guadeloupe in the Caribbean, and the tree fern was found to have suppressed the growth of other ligneous plants. This phenomenon was assumed to be caused by toxic substances released from the fern into the forest floor [2]. However, the substances have not yet been identified, and how those substances are released into the environment is also unknown. Plants 2020, 9, 46; doi:10.3390/plants9010046 www.mdpi.com/journal/plants Plants 2020, 9, x FOR PEER REVIEW 2 of 10 fern into the forest floor [2]. However, the substances have not yet been identified, and how those Plantssubstances2020, 9, 46are released into the environment is also unknown. 2 of 10 Cyathea lepifera (Cyatheaceae) is distributed in the mountains of East and Southeast Asia and growsCyathea up to lepifera15 m high.(Cyatheaceae) The canopy is openness distributed of inthe the fern mountains in the forests of East was and 4-fold Southeast greater Asiathan andtwo growsother closely up to 15 related m high. tree The ferns, canopy C. spinulosa openness and of C. the podophylla. fern in the The forests tree wasferns 4-fold drop greater their old than fronds two otherthrough closely defoliation related and tree ferns,accumulateC. spinulosa on theand forestC. podophylla.floor. The lifeThe span tree fernsof C. droplepifera their fronds old frondsis 6–7 throughmonths, defoliationwhich is significantly and accumulate shorter on than the forest the other floor. two The species life span [3]. of ThoseC. lepifera observationsfronds is suggest 6–7 months, that whichmore fallen is significantly fronds of C. shorter lepifera than accumulate the other on two the species forest floor [3]. Thosethan the observations other two species. suggest that more fallenSeveral fronds tree of C. plants, lepifera suchaccumulate as walnut on and the forestpine, release floor than toxic the substances other two or species. allelopathic substances into theSeveral surrounding tree plants, environment such as walnut through and fallen pine, leaves release [4 toxic–6]. Therefore, substances C. or lepifera allelopathic can be substances studied to intodetermine the surrounding if the tree environmentferns release throughtoxic substances fallen leaves into the [4–6 forest]. Therefore, floor throughC. lepifera defoliationcan be studied of the tofronds. determine The objective if the tree of ferns this releasestudy toxicwas to substances investigate into the the phytotoxicity forest floor through of C. lepifera defoliation fronds of and the fronds.identify The the objectivecompounds of this that study are phytotoxic was to investigate active substances. the phytotoxicity of C. lepifera fronds and identify the compounds that are phytotoxic active substances. 2. Results 2. Results 2.1. Activity of the Extracts of C. lepifera Fronds 2.1. Activity of the Extracts of C. lepifera Fronds The aqueous methanol extracts of the C. lepifera fronds inhibited the root and shoot growth of gardenThe cress, aqueous lettuce, methanol alfalfa, extracts ryegrass of the, timothy,C. lepifera andfronds barnyardgrass inhibited the root(Figure ands shoot 1 and growth 2). The of gardenextract cress,obtained lettuce, from alfalfa, 30 mg ryegrass, of C. lepifera timothy, fronds, and which barnyardgrass was about (Figures 3 ppm1 inand the2). bioassay The extract solution obtained, inhibited from 30garden mg of cress,C. lepifera lettuce,fronds, alfalfa, which ryegrass, was abouttimothy, 3 ppm and in barnyardgrass the bioassay solution,resulting inhibitedin root growth garden ofcress, 0%, lettuce,10.3%, 13.9 alfalfa,%, ryegrass,4.0%, 0% timothy,, and 10.8 and% barnyardgrasscompared with resulting that of incontrol root growth root growth, of 0%, 10.3%, respectively, 13.9%, 4.0%, and 0%,inhibited and 10.8% garden compared cress, lettuce, with that alfalfa, of control ryegrass, root growth,timothy, respectively,and barnyardgrass and inhibited resultinggarden in cress,shoot lettuce,growth alfalfa,of 0%, ryegrass,30.9%, 17.4 timothy,%, 7.4% and, 16.2 barnyardgrass%, and 62.9% resultingcompared in with shoot that growth of control of 0%, shoot 30.9%, growth, 17.4%, 7.4%,respectively. 16.2%, Comparing and 62.9% comparedthe concentrations with that required of control for shoot50% growth growth, inhibitionrespectively. (IC50Comparing value), garden the concentrationscress shoots were required the most for sensitive 50% growth and inhibitionbarnyardgass (IC 50shootsvalue), were garden the least cress sensitive shoots wereto the the extracts most sensitive(Table 1). and barnyardgass shoots were the least sensitive to the extracts (Table1). FigureFigure 1. EEffectsffects of of aqueous aqueous methanol methanol extr extractsacts of C. of lepiferaC. lepifera frondsfronds on the on root the growth root growth of garden of garden cress, cress,lettuce, lettuce, alfalfa, alfalfa, ryegrass, ryegrass, timothy, timothy, and and barnyardgrass barnyardgrass.. Concentrations Concentrations ofof the the tested tested samplessamples correspondedcorresponded toto thethe extractextract obtainedobtained fromfrom 1,1, 3,3, 10,10, 30,30, 100,100, andand 300300 mgmg drydry weight ofof C. lepifera frondsfronds per mL. Means SE from two independent experiments with 10 seedlings for each determination are per mL. Means ±± SE from two independent experiments with 10 seedlings for each determination are shown.shown. DiDifferentfferent lettersletters indicateindicate significantsignificant didifferencesfferences ((pp< < 0.05).0.05). Plants 2020, 9, 46 3 of 10 Plants 2020, 9, x FOR PEER REVIEW 3 of 10 Figure 2.FigureEffects 2. E offfects aqueous of aqueous methanol methanol extracts extracts of ofC. C. lepifera frondsfronds on onthe theshoot shoot growth growth of garden of garden cress, cress, lettuce, alfalfa,lettuce, alfalfa, ryegrass, ryegrass, timothy, timothy, and and barnyardgrass. barnyardgrass. OtherOther details details are are as for as forFigure Figure 1. 1. Table 1.TableThe concentrations1. The concentration of thes of extracts the extracts of C. of lepifera C. lepiferafronds fronds required required for for 50% 50% growthgrowth inhibition (IC50; g dry weight(IC50; g equivalent dry weight equivalent extract per extract mL) per on mL) the rooton the and root shoot and shoot growth growth of of the the test test plants. plants. Root Shoot Root Shoot Garden cress 5.80 a 5.72 a Garden cressLettuce 5.80 a15.4 c 16.8 c 5.72 a LettuceAlfalfa 15.4 c10.7 b 11.3 b 16.8 c Alfalfa Ryegrass 10.7 b7.72 a,b 10.9 b 11.3 b Ryegrass Timothy 7.72 a,b6.47 a,b 12.3 b 10.9 b Timothy Barnyardgrass 6.47 a,b6.74 a,b 44.8 12.3 b BarnyardgrassDifferent letters within the same column6.74 indicatea,b significant differences44.8 (p < 0.05). Different letters within the same column indicate significant differences (p < 0.05). 2.2. Isolation of Active Substances in the C. lepifera Fronds The extract of C. lepifera fronds was separated into ethyl acetate and aqueous fractions. Both 2.2. Isolationfractions of Active suppressed Substances the root in and the shoot C. lepifera growth Fronds of the garden cress seedlings (Figure 3). The ethyl acetate and aqueous fractions obtained from 30 mg of C. lepifera fronds inhibited garden cress Theresulting extract in ofrootC.
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