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Plant rejuvenation: from phenotypes to mechanisms

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Abstract

Plant rejuvenation refers to the reversal of the adult phase in plants and the recovery of part or all of juvenile plant characteristics. The growth and reproductive vitality of plants can be increased after rejuvenation. In recent years, research has successfully reversed the development clock in plants by certain methods; created rejuvenated plants and revealed the basic rules of plant morphology, physiology and reproduction. Here, we reconstitute the changes at the morphological and macromolecular levels, including those in RNA, phytohormones and DNA, during plant rejuvenation. In addition, the characteristics of plant phase changes that can be used as references for plant rejuvenation are also summarized. We further propose possible mechanisms for plant rejuvenation, methods for reversing plant development and problems that should be avoided. Overall, this study highlights the physiological and molecular events involved in plant rejuvenation.

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Abbreviations

ABA:

Abscisic acid

GA3 :

Gibberellin 3

GA4 :

Gibberellin 4

H3K4me3:

Histone H3 lysine 4 trimethylation

H3K27me3:

Histone H3 lysine 27 trimethylation

IAA:

Indole-3-acetic acid

IBA:

4-(Indolyl)-butyric acid

lncRNA:

Long noncoding RNA

miRNA:

MicroRNA

RAGs:

Rejuvenation-associated genes

RA-sRNAs:

Rejuvenation-associated small RNAs

SBP:

Squamosa promoter binding protein

SPL:

SBP-LIKE

sRNAs:

Small RNAs

ZR:

Zeatin riboside

References

  • Ananieva K, Ananiev ED, Mishev K, Georgieva K, Tzvetkova N, Van Staden J (2008) Changes in photosynthetic capacity and polypeptide patterns during natural senescence and rejuvenation of Cucurbita pepo L. (zucchini) cotyledons. Plant Growth Regul 54:23–29

    CAS  Google Scholar 

  • Ashapkin VV, Kutueva LI, Vanyushin BF (2015) Aging epigenetics: accumulation of errors or realization of a specific program? Biochemistry 80:1406–1417

    CAS  PubMed  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and Its APETALA2-like target genes. Plant Cell 15:2730–2741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ay N, Janack B, Humbeck K (2014) Epigenetic control of plant senescence and linked processes. J Exp Bot 65:3875–3887

    PubMed  Google Scholar 

  • Ballester A, Sanjosé MC, Vidal N, Fernándezlorenzo JL, Vieitez AM (1999) Anatomical and biochemical events duringin vitrorooting of microcuttings from juvenile and mature phases of chestnut. Ann Bot 83:619–629

    CAS  Google Scholar 

  • Bastías A, Almada R, Rojas P, Donoso JM, Hinrichsen P, Sagredo B (2016) Aging gene pathway of microRNAs 156/157 and 172 is altered in juvenile and adult plants from in vitro propagated Prunus sp. Cienc Investig Agrar 43:429–441

    Google Scholar 

  • Belostotsky DA, Sieburth LE (2009) Kill the messenger: mRNA decay and plant development. Curr Opin Plant Biol 12:96–102

    CAS  PubMed  Google Scholar 

  • Berthon JY, Boyer N, Gaspar T (1987) Sequential rooting media and rooting capacity of Sequoiadendron giganteum in vitro. Peroxidase activity as a marker. Plant Cell Rep 6:341–344

    CAS  PubMed  Google Scholar 

  • Birnbaum KD, Roudier F (2017) Epigenetic memory and cell fate reprogramming in plants. Regeneration 4:15–20

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bon M, Monteuuis O (1991) Rejuvenation of a 100-year-old Sequoiadendron giganteum through in vitro meristem culture II Biochemical arguments. Physiol Plant 81:116–120

    CAS  Google Scholar 

  • Bonga JM (1987) Clonal propagation of mature trees: problems and possible solutions. For Sci 24–26:249–271

    Google Scholar 

  • Bongard-Pierce DK, Evans MMS, Poethig RS (1996) Heteroblastic features of leaf anatomy in maize and their genetic regulation. Int J Plant Sci 157:331–340

    Google Scholar 

  • Born PV, Rubiosomoza I (2017) Plant miRNA regulation is environmentally and developmentally-sensitive. bioRxiv 136762

  • Brady SM, Sarkar SF, Bonetta D, McCourt P (2003) The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J Cell Mol Biol 34:67–75

    CAS  Google Scholar 

  • Brosché M, Vinocur B, Alatalo ER, Lamminmäki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Triboulot M, Altman A, Polle A, Dreyer E, Rudd S, Paulin L, Auvinen P, Kangasjärvi J (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6:R101

    PubMed  PubMed Central  Google Scholar 

  • Brusslan JA, Bonora G, Rus-Canterbury AM, Tariq F, Jaroszewicz A, Pellegrini M (2015) A genome-wide chronological study of gene expression and two histone modifications, H3K4me3 and H3K9ac, during developmental leaf senescence. Plant Physiol 168:1246–1261

    CAS  PubMed  PubMed Central  Google Scholar 

  • Campisi J, Vijg J (2009) Does damage to DNA and other macromolecules play a role in aging? If so, how? J Gerontol Ser A 64:175–178

    Google Scholar 

  • Cary AJ, Che P, Howell SH (2002) Developmental events and shoot apical meristem gene expression patterns during shoot development in Arabidopsis thaliana. Plant J 32:867–877

    CAS  PubMed  Google Scholar 

  • Chen J, Nolan T, Ye H, Zhang M, Tong H, Xin P (2017) Arabidopsis WRKY46, WRKY54 and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought response. Plant Cell 29:1425–1439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen YT, Shen CH, Lin WD, Chu HA, Huang BL (2013) Small RNAs of Sequoia sempervirens during rejuvenation and phase change. Plant Biol 15:27–36

    CAS  PubMed  Google Scholar 

  • Cierjacks A, Kowarik I, Joshi J, Hempel S, Ristow M, von der Lippe M, Weber E (2013) Biological flora of the british isles: Robinia pseudoacacia. J Ecol 101:1623–1640

    Google Scholar 

  • Cimato A, Cantini C, Sillari B (1990) A method of pruning for the recovery of olive productivity. Intern Symposium on Olive Growing. Acta Horticulturae, Cordoba, pp 251–254

    Google Scholar 

  • Conner AJ, Searle H, Jacobs JME (2019) Rejuvenation of chicory and lettuce plants following phase change in tissue culture. BMC Biotechnol 19:65

    PubMed  PubMed Central  Google Scholar 

  • Crawford BCW, Sewell J, Golembeski G, Roshan C, Long JA, Yanofsky MF (2015) Genetic control of distal stem cell fate within root and embryonic meristems. Science 347:655–659

    CAS  PubMed  Google Scholar 

  • Davenport TL (2006) Pruning strategies to maximize tropical mango production from the time of planting to restoration of old orchards. HortScience 41:544–548

    Google Scholar 

  • Dick JM, Leakey RRB (2006) Differentiation of the dynamic variables affecting rooting ability in juvenile and mature cuttings of cherry (Prunus avium). J Pomol Hortic Sci 81:296–302

    Google Scholar 

  • Du Z, Jia XL, Wang Y, Wu T, Han ZH (2015) Redox homeostasis and reactive oxygen species scavengers shift during ontogenetic phase changes in apple. Plant Sci 236:283–294

    CAS  PubMed  Google Scholar 

  • Dubrovina AS, Kiselev KV (2016) Age-associated alterations in the somatic mutation and DNA methylation levels in plants. Plant Biol 18:185–196

    CAS  PubMed  Google Scholar 

  • Finnegan EJ, Peacock WJ, Dennis ES (2000) DNA methylation, a key regulator of plant development and other processes. Curr Opin Genet Dev 10:217–223

    CAS  PubMed  Google Scholar 

  • Fraga MF, Rodríguez R, Al MC (2002) Genomic DNA methylation–demethylation during aging and reinvigoration of Pinus radiata. Tree Physiol 22:813–816

    CAS  PubMed  Google Scholar 

  • Gao Y, Yang FQ, Cao X, Li CM, Wang Y (2014) Differences in gene expression and regulation during ontogenetic phase change in apple seedlings. Plant Mol Biol Rep 32:357–371

    CAS  Google Scholar 

  • Goebel K (1900) Organography of plants part I. general organography (English translation by I.B. balfour). Clarendon Press, Oxford

  • Greenwood MS (1987) 1. Rejuvenation of forest trees. Plant Growth Regul 6:1–12

    CAS  Google Scholar 

  • Greenwood MS, Day ME, Schatz J (2010) Separating the effects of tree size and meristem maturation on shoot development of grafted scions of red spruce (Picea rubens Sarg.). Tree Physiol 30:459–468

    PubMed  Google Scholar 

  • Guza R, Ma L, Fang Q, Pegg AE, Tretyakova N (2009) Cytosine methylation effects on the repair of O6-methylguanines within CG dinucleotides. J Biol Chem 284:22601–22610

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ha CV, Leyva-Gonzalez MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Dong NV, Yamaguchi-Shinozaki Y, Shinozaki K, Herrera-Estrella L, Tran LP (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci 111:851–856

    PubMed  Google Scholar 

  • Hackett WP, Murray JR, Woo HH, Stapfer RE, Geneve R (1990) Cellular, Biochemical and molecular characteristics related to maturation and rejuvenation in woody species. In: Rodríguez R, Tamés RS, Durzan DJ (eds) NATO ASI. Springer, Boston, 186:147–152

  • Haigis MC, Yankner BA (2010) The aging stress response. Mol Cell 40:333–344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hammatt N, Grant NJ (1993) Apparent rejuvenation of mature wild cherry (Prunus avium L.) during micropropagation. Plant Physiol 141:341–346

    CAS  Google Scholar 

  • He C, Chen X, Huang H, Xu L (2012) Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet 8:e1002911

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoekenga OA, Muszynski MG, Cone KC (2000) Developmental patterns of chromatin structure and DNA methylation responsible for epigenetic expression of a maize regulatory gene. Genetics 155:1889–1902

    CAS  PubMed  PubMed Central  Google Scholar 

  • Högberg KA, Dutkowski GW (2010) Genetic correlations among field trials of Norway spruce clones representing different propagation cycles. Silvae Genetica 59:182–189

    Google Scholar 

  • Holliday R, Grigg GW (1993) DNA methylation and mutation. Mutat Res 285:61–67

    CAS  PubMed  Google Scholar 

  • Huang HJ, Chen Y, Kuo JL, Kuo TT, Tzeng CC, Huang BL, Chen CM, Huang LC (1996) Rejuvenation of Sequoia sempervirens in Vitro: changes in isoesterases and isoperoxidases. Plant Cell Physiol 37:77–80

    CAS  Google Scholar 

  • Huang L, Chow T, Tseng T, Kuo C, Liu S, Ngoh M, Murashige T, Huang H (2003) Association of mitochondrial plasmids with rejuvenation of the coastal redwood, Sequoia sempervirens (D.Don) Endl. Bot Stud 44:25–30

    CAS  Google Scholar 

  • Huang LC, Lius S, Huang BL, Murashige T, El Mahdi FM, Van GR (1992) Rejuvenation of Sequoia sempervirens by repeated grafting of shoot tips onto juvenile rootstocks in vitro: model for phase reversal of trees. Plant Physiol 98:166–173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129

    CAS  PubMed  Google Scholar 

  • Humbeck K (2013) Epigenetic and small RNA regulation of senescence. Plant Mol Biol 82:529–537

    CAS  PubMed  Google Scholar 

  • Husen A (2007) Stock-plant etiolation causes drifts in total soluble sugars and anthraquinones, and promotes adventitious root formation in teak (Tectona grandis L. f.) coppice shoots. Plant Growth Regul 54:13–21

    Google Scholar 

  • Husen A (2011) Rejuvenation and adventitious rooting in coppice-shoot cutting of Tectona grandis as affected by stock-plant etiolation. Am J Plant Sci 2:370–374

    Google Scholar 

  • Ikeuchi M, Shibata M, Rymen B, Iwase A, Bågman A, Watt L, Coleman D, Favero DS, Takahashi T, Ahnert SE, Brady SM, Sugimoto K (2018) A gene regulatory network for cellular reprogramming in plant regeneration. Plant Cell Physiol 59:770–782

    CAS  PubMed Central  Google Scholar 

  • Irish EE, Mcmurray D (2006) Rejuvenation by shoot apex culture recapitulates the developmental increase of methylation at the maize gene Pl-Blotched. Plant Mol Biol 60:747–758

    CAS  PubMed  Google Scholar 

  • Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347

    CAS  PubMed  Google Scholar 

  • Jalakas M, Kelt K, Karp K (2003) The yield and fruit quality of sea buckthorn (Hippophae rhamnoides L.) after rejuvenation cutting. Agron Res 1:31–36

    Google Scholar 

  • Jayaraman J, Miret JA, Munné-Bosch S, Dijkwel PP (2016) Redox and hormone profiling of a Nicotiana tabacum dedifferentiated protoplast culture suggests a role for a cytokinin and gibberellin in plant totipotency. Plant Cell Tissue Organ Cult 124:295–306

    CAS  Google Scholar 

  • Jia XL, Chen YK, Xu XZ, Shen F, Zheng QB (2017) miR156 switches on vegetative phase change under the regulation of redox signals in apple seedlings. Sci Rep 7:14223

    PubMed  PubMed Central  Google Scholar 

  • Kerstetter RA, Poethig RS (1998) The specification of leaf identity during shoot development. Annu Rev Cell Dev Biol 14:373–398

    CAS  PubMed  Google Scholar 

  • Khan M, Rozhon W, Poppenberger B (2014) The role of hormones in the aging of plants—a mini-review. Gerontology 60:49–55

    CAS  PubMed  Google Scholar 

  • Kidner CA, Martienssen RA (2005) The developmental role of microRNA in plants. Curr Opin Plant Biol 8:38–44

    CAS  PubMed  Google Scholar 

  • Kijidani Y, Ohshiro N, Iwata D, Nagamine M, Nishiyama T, Matsumura J, Koga S (2014) Variation of indole acetic acid (IAA) amounts in cambial-region tissues in 7- and 24-year-old sugi (Cryptomeria japonica) trees. J Wood Sci 60:177–185

    CAS  Google Scholar 

  • Koga H, Kaushik S, Cuervo AM (2011) Protein homeostasis and aging: the importance of exquisite quality control. Aging Res Rev 10:205–215

    CAS  Google Scholar 

  • Kovács E, Sárvári É, Nyitrai P, Darók J, Cseh E, Láng F, Keresztes Á (2007) Structural-functional changes in detached cucumber leaves, and modelling these by hormone-treated leaf discs. Plant Biol 9:85–92

    PubMed  Google Scholar 

  • Krupinska K, Falk J, Humbeck K (2003) Genetic, metabolic and environmental factors associated with aging in plants. In: Osiewacz HD (ed) Biology of aging and its modulation Vol 4. Springer, Dordrecht, pp 55–78

  • Kuo T, Kuo J, Huang B, Huang H, Huang L, Cheng C, Chen L (1995) Rejuvenation in vitro: modulation of protein phosphorylation in Sequoia sempervirens. J Plant Physiol 146:333–336

    CAS  Google Scholar 

  • Kuusk V, Niinemets Ü, Valladares F (2018a) A major trade-off between structural and photosynthetic investments operative across plant and needle ages in three Mediterranean pines. Tree Physiol 38:543–557

    PubMed  Google Scholar 

  • Kuusk V, Niinemets Ü, Valladares F (2018b) Structural controls on photosynthetic capacity through juvenile-to-adult transition and needle ageing in Mediterranean pines. Funct Ecol 32:1479–1491

    Google Scholar 

  • Lemmetyinen J, Keinonen-Mettälä K, Lännenpää M, Weissenberg KV, Sopanen T (1998) Activity of the CaMV 35S promoter in various parts of transgenic early flowering birch clones. Plant Cell Rep 18:243–248

    CAS  PubMed  Google Scholar 

  • Li H, Zhao X, Dai H, Wu W, Mao W, Zhang Z (2012) Tissue culture responsive microRNAs in strawberry. Plant Mol Biol Rep 30:1047–1054

    CAS  Google Scholar 

  • Liang C, Wang Y, Zhu Y, Tang J, Hu B, Liu L, Ou S, Wu H, Sun X, Chu J, Chu C (2014) OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proc Natl Acad Sci 111:10013–10018

    CAS  PubMed  Google Scholar 

  • Liu H, Gao Y, Song X, Ma Q, Zhang J, Pei D (2018) A novel rejuvenation approach to induce endohormones and improve rhizogenesis in mature Juglans tree. Plant Methods 14:13

    PubMed  PubMed Central  Google Scholar 

  • Maherali H, Caruso CM, Sherrard ME (2009) The adaptive significance of ontogenetic changes in physiology: a test in Avena barbata. New Phytol 183:908–918

    PubMed  Google Scholar 

  • Masaka K, Torita H, Kon H, Fukuchi M (2017) Seasonality of sprouting in the exotic tree Robinia pseudoacacia L. in Hokkaido, northern Japan. J For Res 20:386–439

    Google Scholar 

  • Massoumi M, Krens FA, Visser RGF, De Klerk GM (2017) Azacytidine and miR156 promote rooting in adult but not in juvenile Arabidopsis tissues. J Plant Physiol 208:52–60

    CAS  PubMed  Google Scholar 

  • Mckeand SE (1988) Optimum age for family selection for growth in genetic tests of loblolly pine. For Sci 34:400–411

    Google Scholar 

  • Mirschel F, Zerbe S, Jansen F (2011) Driving factors for natural tree rejuvenation in anthropogenic pine (Pinus sylvestris L.) forests of NE Germany. For Ecol Manag 261:683–694

    Google Scholar 

  • Mohamed F, Swartz HJ, Buta JG (1991) The role of abscisic acid and plant growth regulators in tissue culture-induced rejuvenation of strawberry ex vitro. Plant Cell Tissue Organ Cult 25:75–84

    CAS  Google Scholar 

  • Moon HK, Park SY, Kim YW, Kim SH (2008) Somatic embryogenesis and plantlet production using rejuvenated tissues from serial grafting of a mature Kalopanax septemlobus tree. Vitro Cell Dev Biol Plant 44:119–127

    CAS  Google Scholar 

  • Morgan DL, Mcwilliams EL, Parr WC (1980) Maintaining juvenility in live oak. HortScience 15:493–494

    Google Scholar 

  • Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195

    CAS  PubMed  Google Scholar 

  • Murch SJ, Campbell SSB, Saxena PK (2001) The role of serotonin and melatonin in plant morphogenesis: Regulation of auxin-induced root organogenesis in in vitro-cultured explants of st. John’s Wort (Hypericum perforatum L.). Vitro Cell Dev Biol Plant 37:786–793

    CAS  Google Scholar 

  • Nascimento B, Sá ACS, Lemos LBD, Rosa DPD, Pereira MDO, Navroski MC (2018) Three epicormic shoot techniques in I. paraguariensis mother trees and its cutting according to the material rejuvenation degree. Cerne 24:240–248

    Google Scholar 

  • Niu SH, Li ZX, Yuan HW, Fang P, Chen XY, Li W (2013) Proper gibberellin localization in vascular tissue is required to regulate adventitious root development in tobacco. J Exp Bot 64:3411–3424

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nyitrai P, Bóka K, Gáspár L, Sárvári E, Keresztes A (2004) Rejuvenation of ageing bean leaves under the effect of low-dose stressors. Plant Biol 6:708–714

    CAS  PubMed  Google Scholar 

  • Nyitrai P, Kovacs E, Kiraly I, Ovari M, Keresztes A (2010) On the mechanism of rejuvenation of ageing detached bean leaves by low-concentration stressors. Plant Biol 11:236–242

    Google Scholar 

  • Ogneva ZV, Dubrovina AS, Kiselev KV (2016) Age-associated alterations in DNA methylation and expression of methyltransferase and demethylase genes in Arabidopsis thaliana. Biol Plant 60:628–634

    CAS  Google Scholar 

  • Peng SL, Tsai CM, Weng CJ (2018) Anti-aging effects of two agricultural plant extracts and their underlying mechanism. In: World Academy of Science, Engineering and Technology. International Journal of Nutrition and Food Engineering, Paris, France, 12:7

  • Perrin Y, Doumas P, Lardets L, Carrons M (1997) Endogenous cytokinins as biochemical markers of rubber-tree (Hevea brasiliensis) clone rejuvenation. Plant Cell, Tissue Organ Cult 47:239–245

    Google Scholar 

  • Peterman TK, Siedow JN (1985) Behavior of lipoxygenase during establishment, senescence, and rejuvenation of soybean cotyledons. Plant Physiol 78:690–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pierik RLM (1990) Rejuvenation and micropropagation. Prog Plant Cell Mol Biol Kluwer Acad 9:91–101

    Google Scholar 

  • Poethig RS (2013) Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105:125–152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poethig RS (2010) The past, present, and future of vegetative phase change. Plant Physiol 154:541–544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poethig RS (1990) Phase change and the regulation of shoot morphogenesis in plants. Science 250:923–930

    CAS  PubMed  Google Scholar 

  • Rando TA, Chang HY (2012) Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 148:46–57

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609–1615

    CAS  PubMed  Google Scholar 

  • Rebecca G, Linan M, Qingming F, Pegg AE, Natalia T (2009) Cytosine methylation effects on the repair of O6-methylguanines within CG dinucleotides. J Biol Chem 284:22601–22610

    Google Scholar 

  • Robertson KD, Jones PA (2000) DNA methylation: past, present and future directions. Carcinogenesis 21:461–467

    CAS  PubMed  Google Scholar 

  • Rédei K, Csiha I, Keserű Z (2011) Black locust (Robinia pseudoacacia L.) short-rotation crops under marginal site conditions. Acta Silvatica et Lignaria Hungarica 7:125–132

    Google Scholar 

  • Salomão LCC, Siqueira DLD, Silva DFPD (2018) Production of ‘Ubá’ mango tree submitted to rejuvenation pruning and fertilized with nitrogen. Revista Brasileira De Fruticultura 40:e812

    Google Scholar 

  • Shanthi K, Bachpai VKW, Anisha S, Ganesan M, Anithaa RG, Subashini V, Chakravarthi M, Sivakumar V, Yasodha R (2015) Micropropagation of Eucalyptus camaldulensis for the production of rejuvenated stock plants for microcuttings propagation and genetic fidelity assessment. New For 46:357–371

    Google Scholar 

  • Skadsen RW, Cherry JH (1983) Quantitative changes in in vitro and in vivo protein synthesis in aging and rejuvenated soybean cotyledons. Plant Physiol 71:861–868

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steward FC, Mapes MO, Mears K (1958) Growth and organized development of cultured cells. II. Organization in cultures grown from freely suspended cell. Am J Bot 45:705–708

    Google Scholar 

  • Sumin L, Sujeoung S, Seju K, Crain RC, Myoung K, Honggil N, Youngsook L, Lee SM (2010) Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. Plant J 12:547–556

    Google Scholar 

  • Takeno K, Ise H, Minowa H, Dounowaki T (1992) Fruit growth induced by benzyladenine in Cucumis sativus L.: influence of benzyladenine on cell division, cell enlargement and indole3-acetic acid content. Engei Gakkai zasshi 60:915–920

    CAS  Google Scholar 

  • Teotia S, Tang G (2015) To bloom or not to bloom: role of microRNAs in plant flowering. Mol Plant 8:359–377

    CAS  PubMed  Google Scholar 

  • Thokchom R, Sharma DP, Thakur KK (2018) Effect of rejuvenation pruning and nitrogen levels on leaf nutrient status of old and senile apricot (Prunus armeniaca L.) cv. new castle trees. Int J Curr Microbiol Appl Sci 7:2492–2500

    Google Scholar 

  • Tschaplinski TJ, Blake TJ (1989) Photosynthetic reinvigoration of leaces following shoot decapitation and accelerated growth of coppice shoots. Physiol Plant 75:157–165

    Google Scholar 

  • Vaucheret H (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18:1187–1197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Venkatarayappa T, Fletcher RA, Thompson JE (1984) Retardation and reversal of senescence in bean leaves by benzyladenine and decapitation. Plant Cell Physiol 25:407–418

    CAS  Google Scholar 

  • Voß U, Wilson MH, Kenobi K, Gould PD, Robertson FC, Peer WA, Lucas M, Swarup K, Casimiro I, Holman TJ, Wells DM, Péret B, Goh T, Fukaki H, Hodgman TC, Laplaze L, Halliday KJ, Ljung K, Murphy AS, Hall AJ, Webb AAR, Bennett MJ (2015) The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat Commun 6:7641

    PubMed  PubMed Central  Google Scholar 

  • Wang J, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    CAS  PubMed  Google Scholar 

  • Wang JW (2014) Regulation of flowering time by the miR156-mediated age pathway. J Exp Bot 65:4723–4730

    CAS  PubMed  Google Scholar 

  • Wang JW, Park MY, Wang LJ, Koo Y, Chen XY, Weigel D, Poethig RS (2011) MiRNA control of vegetative phase change in trees. PLoS Genet 7:e1002012

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wang Y, Zhao YB, Chen DM, Han ZH (2014) Protein phosphorylation differs significantly among ontogenetic phases in Malus seedlings. Proteome Sci 12:12–31

    Google Scholar 

  • Wang Y, Yao RL (2019) Increased endogenous indole-3-acetic acid:abscisic acid ratio is a reliable marker of Pinus massoniana rejuvenation. Biotech Histochem 94:1–8

    Google Scholar 

  • Webster CA, Jones OP (1989) Micropropagation of the apple rootstock M.9: effect of sustained subculture on apparent rejuvenation in vitro. J Hortic Sci 64:421–428

    Google Scholar 

  • Wendling I, Brondani GE, Biassio AD, Dutra LF (2013) Vegetative propagation of adult Ilex paraguariensis trees through epicormic shoots. Acta Sci-Agron 35:117–125

    CAS  Google Scholar 

  • Wilhelmová N, Fuksová H, Srbová M, Miková D, Mýtinová Z, Procházková D, Vytásek R, Wilhelm J (2006) The effect of plant cytokinin hormones on the production of ethylene, nitric oxide, and protein nitrotyrosine in ageing tobacco leaves. BioFactors 27:203–211

    PubMed  Google Scholar 

  • Willson MF (1981) On the evolution of complex life cycles in plants: a review and an ecological perspective. Ann Mo Bot Gard 68:275–300

    Google Scholar 

  • Wu G, Park MY, Conway SR, Wang J, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao Z, Ji N, Zhang X, Zhang Y, Wang Y, Wu T, Xu X, Han Z (2014) The lose of juvenility elicits adventitious rooting recalcitrance in apple rootstocks. Plant Cell Tissue Organ Cult 119:51–63

    Google Scholar 

  • Xu M, Hu T, Zhao J, Park M, Earley KW, Wu G, Yang L, Poethig RS (2016) Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. PLoS Genet 12:e1006263

    PubMed  PubMed Central  Google Scholar 

  • Ye BB, Zhang K, Wang JW (2019) The role of miR156 in rejuvenation in Arabidopsis thaliana. J Integr Plant Biol 00:1–6

    Google Scholar 

  • Yeom M, Kim H, Lim J, Shin A, Hong S, Kim J, Nam HG (2014) How do phytochromes transmit the light quality information to the circadian clock in Arabidopsis ? Mol Plant 7:1701–1704

    CAS  PubMed  Google Scholar 

  • Yu S, Lian H, Wang J (2015) Plant developmental transitions: the role of microRNAs and sugars. Curr Opin Plant Biol 27:1–7

    PubMed  Google Scholar 

  • Yuan JL, Sun HM, Guo GP, Yue JJ, Gu XP (2014) Correlation between DNA methylation and chronological age of Moso bamboo (Phyllostachys heterocycla var. pubescens). Bot Stud 55:4

    PubMed  PubMed Central  Google Scholar 

  • Zhang G, Zhao F, Chen L, Pan Y, Sun L, Bao N, Zhang T, Cui C, Qiu Z, Zhang Y, Yang L, Xu L (2019) Jasmonate-mediated wound signalling promotes plant regeneration. Nat Plants 5:491–497

    CAS  PubMed  Google Scholar 

  • Zhang YC, Chen YQ (2013) Long noncoding RNAs: new regulators in plant development. Biochem Biophys Res Commun 436:111–114

    CAS  PubMed  Google Scholar 

  • Zluvova J, Janousek B, Vyskot B (2001) Immunohistochemical study of DNA methylation dynamics during plant development. J Exp Bot 52:2265–2273

    CAS  PubMed  Google Scholar 

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Funding

This study was funded by the Long-Term Research Program for Young Teachers of Beijing Forestry University (2015ZCQ-SW-03), the National Natural Science Foundation of China (31570677), and the National Key R&D Program of China (2017YFD0600503).

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Authors and Affiliations

  1. Beijing Advanced Innovation Center for Tree Breeding By Molecular Design, Engineering Technology Research Center of Black Locust of National Forestry and Grassland Administration, National Engineering Laboratory For Tree Breeding, College of Biological Science and Technology, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Zijie Zhang, Yuhan Sun & Yun Li

Authors
  1. Zijie Zhang
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  2. Yuhan Sun
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  3. Yun Li
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Contributions

ZZ and YL conceived and designed the review. ZZ and YS wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Yun Li.

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Communicated by Neal Stewart.

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Zhang, Z., Sun, Y. & Li, Y. Plant rejuvenation: from phenotypes to mechanisms. Plant Cell Rep 39, 1249–1262 (2020). https://doi.org/10.1007/s00299-020-02577-1

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