Abstract
The rapid stem elongation of the invasive weed Mikania micrantha in the forest understory is of vital significance for its successful invasion. To understand the physiological and molecular mechanisms for this process, here we comparatively investigated the physiological characteristics and transcriptome patterns of M. micrantha stem under low light (30%) and full light (100%) conditions. The results showed that M. micrantha stem had photosynthetic capacity, which was highly plastic to light intensities, constituting an indispensable part of the plastic response of M. micrantha to shading. M. micrantha had longer internodes, epidermal cells, and consequently longer stems under low light than full light conditions, which could proximally be attributed to phytohormone production and reduction of photoprotective substances as potential metabolic trade-off, as observed here under shading treatment. The transcriptome sequencing and qPCR verified the results from physiological investigation, and showed that under low light condition the expression levels of genes involved in photosynthesis (e.g. MmPsaA, MmPsbO1 and MmFd3) were generally down-regulated in comparison to full light condition, as were genes related to the photoprotective substances synthesis (e.g. MmCHS, and MmF3H1) and the negative regulators of phytohormone (e.g. MmAUX1, MmRR1 and MmGAI). It was concluded that the regulation of phytohormones and photoprotective substances are important material basis for the rapid elongation of M. micrantha stems with high plasticity, which facilitates the vine's invasiveness in the forest understory.
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DNA sequences related to this study have been uploaded to NCBI database, NCBI SRA: LL1-LL3: SRR10810951, SRR10810952, SRR10810953; FL1-FL3: SRR10810958, SRR10810949, SRR10810940. Other data supporting the findings of this study are available within the paper and its supplementary files.
References
Agati G, Brunetti C, Di Ferdinando M, Ferrini F, Pollastri S, Tattini M (2013) Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiol Biochem 72:35–45. https://doi.org/10.1016/j.plaphy.2013.03.014
Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106. https://doi.org/10.1186/gb-2010-11-10-r106
Arnold PA, Kruuk LEB, Nicotra AB (2019) How to analyse plant phenotypic plasticity in response to a changing climate. New Phytol 222:1235–1241. https://doi.org/10.1111/nph.15656
Aschan G, Pfanz H (2003) Non-foliar photosynthesis – a strategy of additional carbon acquisition. Flora Elsevier GmbH 198:81–97. https://doi.org/10.1078/0367-2530-00080
Aschan G, Pfanz Z, Vodnik D, Batic F (2005) Photosynthetic performance of vegetative and reproductive structures of green hellebore (Helleborus viridis L.agg.). Photosynthetica 43:55–64. https://doi.org/10.1007/s11099-005-5064-x
Banerjee AK, Dewanji A (2017) Role of intraspecific trait plasticity in Mikania micrantha Kunth growth and impact of its abundance on community composition. J Asia Pac Biodivers 10:237–249. https://doi.org/10.1016/j.japb.2017.04.003
Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155. https://doi.org/10.1016/s0065-2660(08)60048-6
Bricker TM, Frankel LK (2008) The psbo1 mutant of Arabidopsis cannot efficiently use calcium in support of oxygen evolution by photosystem II. J Biol Chem 283:29022–29027. https://doi.org/10.1074/jbc.M805122200
Carabelli M, Possenti M, Sessa G, Ruzza V, Morelli G, Ruberti I (2018) Arabidopsis HD-Zip II proteins regulate the exit from proliferation during leaf development in canopy shade. J Exp Bot 69:5419–5431. https://doi.org/10.1093/jxb/ery331
Casal JJ (2013) Photoreceptor signaling networks in plant responses to shade. Annu Rev Plant Biol 64:403–427. https://doi.org/10.1146/annurev-arplant-050312-120221
Cerrudo I et al (2012) Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiol 158:2042–2052. https://doi.org/10.1104/pp.112.193359
Chevin LM, Hoffmann AA (2017) Evolution of phenotypic plasticity in extreme environments. Philos Trans R Soc Lond B Biol Sci 372:20160138. https://doi.org/10.1098/rstb.2016.0138
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431. https://doi.org/10.1111/j.1461-0248.2011.01596.x
Day MD et al (2012) Mikania micrantha Kunth (Asteraceae) (mile-a-minute): its distribution and physical and socioeconomic impacts in Papua New Guinea. Pac Sci 66:213–223. https://doi.org/10.2984/66.2.8
Day MD et al (2016) Biology and impacts of pacific islands invasive species. 13. Mikania micrantha Kunth (Asteraceae). Pac Sci 70:257–285. https://doi.org/10.2984/70.3.1
De Roo L, Roberto LS, Steppe K (2020) Woody tissue photosynthesis reduces stem CO2 efflux by half and remains unaffected by drought stress in young Populus tremula trees. Plant Cell Environ 43:981–991
De Wit M, Galvao VC, Fankhauser C (2016) Light-mediated hormonal regulation of plant growth and development. Annu Rev Plant Biol 67:2221–2225. https://doi.org/10.1146/annurev-arplant-043015-112252
Deng X (2010) Morphological and physiological plasticity responding to different light environments of the invasive plant, Mikania micrantha H.B.Kunth. Ecol Environ 19:1170–1175. https://doi.org/10.16258/j.cnki.1674-5906.2010.05.037
Flory SL, Clay LK (2011) Invasive microstegium populations consistently outperform native range populations across diverse environments. Ecology 92:2248–2257. https://doi.org/10.1016/j.baae.2011.02.013
Floß B, Igloi GL, Cassier-Chauvat C, Muhlenhoff U (1997) Molecular characterization and overexpression of the petF gene from Synechococcus elongatus: evidence for a second site of electrostatic interaction between ferredoxin and the PS I-D subunit. Photosynth Res 54:63–71. https://doi.org/10.1023/A:1005823620291
Han DD, Wang LY, Luo YP (2018) Isolation, identification, and the growth promoting effects of two antagonistic actinomycete strains from the rhizosphere of Mikania micrantha Kunth. Microbiol Res 208:1–11. https://doi.org/10.1016/j.micres.2018.01.003
Heimler D, Vignolini P, Dini MG, Romani A (2005) Rapid tests to assess the antioxidant activity of Phaseolus vulgaris L. Dry Beans J Agric Food Chem 53:3053–3056. https://doi.org/10.1021/jf049001r
Henery ML et al (2010) Evidence for a combination of pre-adapted traits and rapid adaptive change in the invasive plant Centaurea stoebe. J Ecol 98:800–813. https://doi.org/10.1111/j.1365-2745.2010.01672.x
Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci 18:477–483. https://doi.org/10.1016/j.tplants.2013.06.003
Julian MH, Quick WP (2002) Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415:451–454. https://doi.org/10.1038/415451a
Kanehisa M et al (2007) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484. https://doi.org/10.1093/nar/gkm882
Kaur R, Malhotra S (2011) Effects of invasion of Mikania micrantha on germination of rice seedlings, plant richness, chemical properties and respiration of soil. Biol Fertil Soils 48:481–488. https://doi.org/10.1007/s00374-011-0645-2
Kim J, Eichacker LA, Rudiger W, Mulle JE (1994) Chlorophyll regulates accumulation of the plastid-encoded chlorophyll proteins P700 and D1 by lncreasing apoprotein stability. Plant Physiol 104:907–916. https://doi.org/10.1097/CCM.0b013e318270e7bd
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360. https://doi.org/10.1038/nmeth.3317
Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol Plant 86:180–187. https://doi.org/10.1111/j.1399-3054.1992.tb01328.x
Lane BG, Dunwelll JM, Rag JA, Schmitt MR, Cumin AC (1993) Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 268:12239–12242. https://doi.org/10.1111/j.1432-1033.1993.tb17998.x
Li HP (2009) Plant microscopy, 2nd edn. Science Press, Beijing
Li MG et al (2012) Evaluation of the controlling methods and strategies for Mikania micrantha H. B. K. Acta Ecol Sin 32:3240–3251. https://doi.org/10.5846/stxb201104090460
Li XQ, Zhang FL, Yang T, Zhe GX, Mao CL, Wu Y (2019) Effect of shading on leaf morphology and photosynthetic parameters in endangered Horsfieldia glabra seedlings. J Plant Physiol 55:80–90. https://doi.org/10.13592/j.cnki.ppj.2018.0369
Liu Y, Qian CY, Ding SH, Shang XL, Yang WX, Fang SZ (2016) Effect of light regime and provenance on leaf characteristics, growth and flavonoid accumulation in Cyclocarya paliurus (Batal) Iljinskaja coppices. Bot Stud 57:28. https://doi.org/10.1186/s40529-016-0145-7
Liu B et al (2020) Mikania micrantha genome provides insights into the molecular mechanism of rapid growth. Nat Commun 11:340. https://doi.org/10.1038/s41467-019-13926-4
Ma ZL, Yang WQ, Wu FZ, Gao S (2014) Effects of shading on the aboveground biomass and stiochiometry characteristics of Medicago. Chin J Appl Ecol 25:3139–3144. https://doi.org/10.13287/j.1001-9332.20140829.010
Ma ZL, Gao S, Yang WQ, Zhu P, Wu FZ, Tan B (2015) Effects of shading treatments on biomass and nutrient accumulation of herb community in abandoned land in the subtropical region. Acta Ecol Sin 35:5279–5286. https://doi.org/10.5846/stxb201402240315
Macanawai A, Day M, Tumaneng-Diete T, Adkins S (2012) Impact of Mikania micrantha on crop production systems in Viti Levu. Fiji Pak J Weed Sci Res 18:357–365. http://espace.library.uq.edu.au/view/UQ:297497
Manrique V, Diaz R, Cuda JP, Overholt WA (2011) Suitability of a new plant invader as a target for biological control in Florida. Invasive Plant Sci Manag 4:1–10. https://doi.org/10.1614/ipsm-d-10-00040.1
Mao PL, Zang RG, Shao HB, Yu JB (2014) Functional trait trade-offs for the tropical montane rain forest species responding to light from simulating experiments. Sci World J 2014:649031. https://doi.org/10.1155/2014/649031
Mathur S, Jain L, Jajoo A (2018) Photosynthetic efficiency in sun and shade plants. Photosynthetica 56:354–365. https://doi.org/10.1007/s11099-018-0767-y
McGeoch MA et al (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108. https://doi.org/10.1111/j.1472-4642.2009.00633.x
Nakayama H, Sinha NR, Kimura S (2017) How do plants and phytohormones accomplish heterophylly, leaf phenotypic plasticity, in response to environmental cues. Front Plant Sci 8:1717. https://doi.org/10.3389/fpls.2017.01717
Owens DK, Crosby KC, Runac J, Howard BA, Winkel BS (2008) Biochemical and genetic characterization of Arabidopsis flavanone 3beta-hydroxylase. Plant Physiol Biochem 46:833–843. https://doi.org/10.1016/j.plaphy.2008.06.004
Palacio-López K, Gianoli E (2011) Invasive plants do not display greater phenotypic plasticity than their native or non-invasive counterparts: a meta-analysis. Oikos 120:1393–1401. https://doi.org/10.1111/j.1600-0706.2010.19114.x
Qin RM et al (2012) The evolution of increased competitive ability, innate competitive advantages, and novel biochemical weapons act in concert for a tropical invader. New Phytol 197:979–988. https://doi.org/10.1111/nph.12071
Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62. https://doi.org/10.1007/BF00024185
Sessa G, Carabelli M, Possenti M, Morelli G, Ruberti I (2018) Multiple pathways in the control of the shade avoidance response. Plants (basel) 7:102. https://doi.org/10.3390/plants7040102
Shi YY, Tian SW, Hou LY, Huang XZ, Zhang XY, Guo HW, Yang SH (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24:2578–2595. https://doi.org/10.1105/tpc
Simberloff D et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013
Singh M, Gupta A, Singh D, Khurana JP, Laxmi A (2017) Arabidopsis RSS1 mediates cross-talk between glucose and light signaling during hypocotyl elongation growth. Sci Rep 7:16101. https://doi.org/10.1038/s41598-017-16239-y
Stamm P, Kumar PP (2010) The phytohormone signal network regulating elongation growth during shade avoidance. J Exp Bot 61:2889–2903. https://doi.org/10.1093/jxb/erq147
Sun CD, Huang HZ, Xu CJ, Li X, Chen KS (2013) Biological activities of extracts from Chinese bayberry (Myrica rubra Sieb. et Zucc.): a review. Plant Food Hum Nutr 68:97–106. https://doi.org/10.1007/s11130-013-0349-x
Swarup R, Bhosale R (2019) Developmental roles of AUX1/LAX auxin influx carriers in plants. Front Plant Sci 10:1306. https://doi.org/10.3389/fpls.2019.01306
Tang YJ, Liesche J (2017) The molecular mechanism of shade avoidance in crops—how data from Arabidopsis can help to identify targets for increasing yield and biomass production. J Integr Agric 16:1244–1255. https://doi.org/10.1016/s2095-3119(16)61434-x
Trapnell C et al (2010) Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. https://doi.org/10.1038/nbt.1621
Tyler L, Thomas SG, Hu JH, Dill A, Alonso JM, Ecker JR, Sun TP (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019. https://doi.org/10.1104/pp.104.039578
Vijayan S, Joy CM (2017) Properties of natural fibers separated from chromolaena odorata and Mikania micrantha. J Nat Fibers 15:1–10. https://doi.org/10.1080/15440478.2017.1330720
Wan JZ et al (2020) Can polyploidy confer invasive plants with a wider climatic tolerance? A test using Solidago canadensis. Ecol Evol 10:1–14. https://doi.org/10.1002/ece3.6303
Wei W, Hou YP, Peng SL, Chen PD, Liang XP, Zhang J (2017) Effects of light intensity on growth and biomass allocation of invasive plants Mikania micrantha and Chromolaena odorata. Acta Ecol Sin 37:6021–6028. https://doi.org/10.5846/stxb201606301343
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/s0176-1617(11)81192-2
Wen DZ, Ye WH, Feng HL, Cai CX (2000) Comiparison of basic photosynthetic characteristics between exotic invader weed Mikania micrantha and its companion species. J Trop Subtrop Bot 8:139–146. https://doi.org/10.3969/j.issn.1005-3395.2000.2.010
Xie XZ, Xue YJ, Zhou JJ, Zhang B, Chang H, Takano M (2011) Phytochromes regulate SA and JA signaling pathways in rice and are required for developmentally controlled resistance to Magnaporthe grisea. Mol Plant 4:688–696. https://doi.org/10.1093/mp/ssr005
Xu DH, Fang XW, Su PX, Wang G (2012) Ecophysiological responses of Caragana korshinskii Kom. under extreme drought stress: Leaf abscission and stem survives. Photosynthetica 50:541–548. https://doi.org/10.1007/s11099-012-0060-4
Xuan LJ et al (2018) TRANSPARENT TESTA 4-mediated flavonoids negatively affect embryonic fatty acid biosynthesis in Arabidopsis. Plant Cell Environ 41:2773–2790. https://doi.org/10.1111/pce.13402
Yang JC, Zhang JH, Wang ZQ, Zhu QS, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323. https://doi.org/10.1104/pp.127.1.315
Yang CJ, Liu JJ, Dong XR, Cai ZY, Tian WD, Wang XL (2014) Short-term and continuing stresses differentially interplay with multiple hormones to regulate plant survival and growth. Mol Plant 7:841–855. https://doi.org/10.1093/mp/ssu013
Yin JL et al (2020) Carbohydrate, phytohormone, and associated transcriptome changes during storage root formation in Alternanthera philoxeroides. Weed Sci 68:1–39. https://doi.org/10.1017/wsc.2020.37
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14. https://doi.org/10.1186/gb-2010-11-2-r14
Zan QJ, Wang YJ, Wang BS, Liao WB, Li MG (2000) The Distribution and Harm of the Exotic Weed Mikania Micrantha. Chin J Ecol 19:58–61. https://doi.org/10.13292/j.1000
Zhang LY, Ye WH, Cao HL, Feng HL (2004) Mikania micrantha H. B. K. in China—an overview. Weed Res 44:42–49. https://doi.org/10.1111/j.1365-3180.2003.00371.x
Zhang ZY, Zhang ZJ, Pan XY (2015) Phenotypic plasticity of Alternanthera philoxeroides in response to shading: introduced vs. native populations. Biodiv Sci 23:18–22. https://doi.org/10.17520/biods.2014065
Zhang TJ, Chow WS, Liu XT, Peng Z, Liu N, Peng CL (2016) A magic red coat on the surface of young leaves: anthocyanins distributed in trichome layer protect Castanopsis fissa leaves from photoinhibition. Tree Physiol 36:1296–1306. https://doi.org/10.1093/treephys/tpw080
Zhang TJ, Zheng J, Yu ZC, Gu XQ, Tian XS, Peng CL, Chow WS (2017) Variations in photoprotective potential along gradients of leaf development and plant succession in subtropical forests under contrasting irradiances. Environ Exp Bot 154:23–32. https://doi.org/10.1016/j.envexpbot.2017.07.016
Zhang TJ et al (2018) Functional characteristics of phenolic compounds accumulated in young leaves of two subtropical forest tree species of different successional stages. Tree Physiol 38:1486–1501. https://doi.org/10.1093/treephys/tpy030
Zhu HF et al (2017) Effects of low light on photosynthetic properties, antioxidant enzyme activity, and anthocyanin accumulation in purple pak-choi (Brassica campestris ssp. Chinensis Makino). PLoS ONE 12:e0179305. https://doi.org/10.1371/journal.pone.0179305
Zu YG, Zhang ZH, Wang WJ, Yang FJ, He HS (2006) Different characteristics of photosynthesis in stems and leaves of Mikania micranth. Chin J Plant Ecol 30:998–1004. https://doi.org/10.17521/cjpe.2006.0128
Acknowledgements
We thank Johannes J. Le Roux (Macquarie University), Bo Liu and Wei Fan (Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences) for constructive comments on the manuscript.
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This research was supported by the National Key Research and Development Program of China (Grant No. 2017YFC1200105).
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WL planned and designed the experiment. ZJ and YZ performed the experiment. ZJ, YW and MC analyzed the data, and ZJ wrote the original manuscript. YW and WL made great contributions to the revision. CP commented on the manuscript and supported this research.
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Jiang, Z., Wang, Y., Zheng, Y. et al. Physiological and transcriptomic responses of Mikania micrantha stem to shading yield novel insights into its invasiveness. Biol Invasions 23, 2927–2943 (2021). https://doi.org/10.1007/s10530-021-02546-z
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DOI: https://doi.org/10.1007/s10530-021-02546-z