Rejuvenation increases leaf biomass and flavonoid accumulation in Ginkgo biloba

Zhaogeng Lu , Likui Zhu , Jinkai Lu , Nan Shen , Lu Wang , Sian Liu , Qingjie Wang , Wanwen Yu , Hisashi Kato-Noguchi , Weixing Li , Biao Jin , Li Wang , Jinxing Lin

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhab018

PDF (3672KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhab018 DOI: 10.1093/hr/uhab018
Article
research-article
Rejuvenation increases leaf biomass and flavonoid accumulation in Ginkgo biloba
Author information +
History +
PDF (3672KB)

Abstract

Rejuvenation refers to the transition from an adult state to a juvenile state. Trunk truncation at the base of the tree can result in tree rejuvenation. However, little is known about the association of rejuvenation with leaf biomass and flavonoid accumulation. The results of this study showed that, compared with control leaves, leaves of renewed Ginkgo biloba shoots were larger, thicker, and more lobed and had higher fresh/dry weights and chlorophyll contents. The leaf biomass per hectare of rejuvenated trees was twofold higher than that of the untruncated controls. Moreover, we observed a marked increase in the accumulation of flavonol glycosides via metabolomic analysis and detected upregulated expression of genes involved in flavonoid biosynthesis, including CHS, FLS, F3’H, DFR, and LAR. Overexpression of GbCHS in ginkgo calli confirmed that GbCHS plays an important role in flavonoid biosynthesis. Interestingly, the contents of gibberellins significantly increased in the rejuvenated leaves. Moreover, exogenous gibberellin treatment significantly increased GbCHS expression and flavonoid contents. Our findings show that truncation can stimulate tree rejuvenation by altering hormone levels, representing an effective and feasible approach for enhancing the biomass and flavonoid content of G. biloba leaves.

Cite this article

Download citation ▾
Zhaogeng Lu, Likui Zhu, Jinkai Lu, Nan Shen, Lu Wang, Sian Liu, Qingjie Wang, Wanwen Yu, Hisashi Kato-Noguchi, Weixing Li, Biao Jin, Li Wang, Jinxing Lin. Rejuvenation increases leaf biomass and flavonoid accumulation in Ginkgo biloba. Horticulture Research, 2022, 9 (1) : uhab018 DOI:10.1093/hr/uhab018

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Greenwood MS . Juvenility and maturation in conifers, current concepts. Tree Physiol. 1995; 15: 433-8.

[2]

Pei D, Gu R . A review on the rejuvenation of mature trees. Chine Bull Bot. 2005; 22: 753-60.

[3]

Poethig RS . The past, present, and future of vegetative phase change. Plant Physiol. 2010; 154: 541-4.

[4]

Barthelemy D, Caraglio Y . Plant architecture: a dynamic, multi-level and comprehensive approach to plant form, structure and ontogeny. Ann Bot. 2007; 99: 375-407.

[5]

Heide OM . Juvenility, maturation and rejuvenation in plants, adventitious bud formation as a novel rejuvenation process. J Hortic Sci Biotechnol. 2019; 94: 2-11.

[6]

Zhang Z, Sun Y, Li Y . Plant rejuvenation: from phenotypes to mechanisms. Plant Cell Rep. 2020; 39: 1249-62.

[7]

Wang JW, Park MY, Wang L-J et al. miRNA control of vegetative phase change in trees. PLoS Genet. 2011; 7: e1002012.

[8]

Wendling I, Trueman SJ, Xavier A . Maturation and related aspects in clonal forestry-part I: concepts, regulation and consequences of phase change. New For. 2014b; 45: 449-71.

[9]

Wendling I, Trueman SJ, Xavier A . Maturation and related aspects in clonal forestry-part II: reinvigoration, rejuvenation and juvenility maintenance. New For. 2014a; 45: 473-86.

[10]

Ford YY, Taylor JM, Blake PS et al. GibberellinA3 stimulates adventitious rooting of cuttings from cherry (Prunus avium). Plant Growth Regul. 2002; 37: 127-33.

[11]

Gordon SP, Heisler MG, Venugopala G et al. Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development. 2007; 134: 3539-48.

[12]

Sun T . The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol. 2011; 21: R338-45.

[13]

Hackett WP . Juvenility, maturation and rejuvenation in woody plants. Hortic Rev. 1985; 7: 109-55.

[14]

Evans MM, Poethig RS . Gibberellins promote vegetative phase change and reproductive maturity in maize. Plant Physiol. 1995; 108: 475-87.

[15]

Manuela D, Xu M . Juvenile leaves or adult leaves: determinants for vegetative phase change in flowering plants. Int J Mol Sci. 2020; 21: 9753.

[16]

Telfer A, Poethig RS . HASTY: a gene that regulates the timing of shoot maturation in Arabidopsis thaliana. Development. 1998; 125: 1889-98.

[17]

Tanaka N. Gibberellin is not a regulator of miR156 in rice juvenile-adult phase change. Rice. 2012; 5: 25.

[18]

Lauter N, Kampani A, Carlson SR et al. microRNA172 downregulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci U S A. 2005; 102: 9412-7.

[19]

Zhang T, Lian H, Tang H et al. An intrinsic microRNA timer regulates progressive decline in shoot regenerative capacity in plants. Plant Cell. 2015; 27: 349-60.

[20]

Ye BB, Zhang K, Wang JW . The role of miR156 in rejuvenation in Arabidopsis thaliana. J Integr Plant Biol. 2020; 62: 550-5.

[21]

Wang JW, Czech B, Weigel D . miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell. 2009; 138: 738-49.

[22]

Yu S, Galvao VC, Zhang Y-C et al. Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA promoter binding-like transcription factors. Plant Cell. 2012; 24: 3320-32.

[23]

Ahsan MU, Hayward A, Irihimovitch V et al. Juvenility and vegetative phase transition in tropical/subtropical tree crops. Front Plant Sci. 2019; 10: 729.

[24]

Yang L, Xu M, Koo Y et al. Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. elife. 2013; 2: e00260.

[25]

Yu S, Cao L, Zhou C-M et al. Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. elife. 2013; 2: e00269.

[26]

Ponnu J, Schlereth A, Zacharaki V et al. The Trehalose 6-phosphate pathway impacts vegetative phase change in Arabidopsis thaliana. Plant J. 2020; 104: 768-80.

[27]

Buer CS, Imin N, Djordjevic MA . Flavonoids: new roles for old molecules. J Integr Plant Biol. 2010; 52: 98-111.

[28]

Feller A, Machemer K, Braun EL et al. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J. 2011; 66: 94-116.

[29]

Xu W, Dubos C, Lepiniec L . Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci. 2015; 20: 176-85.

[30]

Yu Z-X, Wang L-J, Zhao B et al. Progressive regulation of sesquiterpene biosynthesis in Arabidopsis and patchouli (Pogostemon cablin) by the miR156-targeted SPL transcription factors. Mol Plant. 2015; 8: 98-110.

[31]

Mao Y-B, Liu Y-Q, Chen D-Y et al. Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance. Nat Commun. 2017; 8: 1-13.

[32]

Gou J, Felippes FF, Liu C et al. Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell. 2011; 23: 1512-22.

[33]

Zhao Y-P, Fan G, Yin P-P et al. Resequencing 545 ginkgo genomes across the world reveals the evolutionary history of the living fossil. Nat Commun. 2019; 10: 4201.

[34]

Liu H, Wang X, Wang G et al. The nearly complete genome of Ginkgo biloba illuminates gymnosperm evolution. Nat Plants. 2021; 7: 748-56.

[35]

Lu J, Xu Y, Meng Z et al. Integration of morphological, physiological and multi-omics analysis reveals the optimal planting density improving leaf yield and active compound accumulation in Ginkgo biloba. Ind Crop Prod. 2021; 172: 114055.

[36]

Zhang H-F, Huang L-B, Zhong Y-B et al. An overview of systematic reviews of Ginkgo biloba extracts for mild cognitive impairment and dementia. Front Aging Neurosci. 2016; 8: 276.

[37]

Zuo W, Yan F, Zhang B et al. Advances in the studies of Ginkgo biloba leaves extract on aging-related diseases. Aging Dis. 2017; 8: 812-26.

[38]

Shu Z, Shar AH, Shahen M et al. Pharmacological uses of Ginkgo biloba extracts for cardiovascular disease and coronary heart diseases. Int J Pharmacol. 2019; 15: 1-9.

[39]

Singh SK, Srivastav S, Castellani RJ et al. Neuroprotective and antioxidant effect of Ginkgo biloba extract against AD and other neurological disorders. Neurotherapeutics. 2019; 16: 666-74.

[40]

Momtazi-Borojeni AA, Katsiki N, Pirro M et al. Dietary natural products as emerging lipoprotein(a)-lowering agents. J Cell Physiol. 2019; 234: 12581-94.

[41]

Yao X, Shang E, Zhou G et al. Comparative characterization of total flavonol glycosides and terpene lactones at different ages, from different cultivation sources and genders of Ginkgo biloba leaves. Int J Mol Sci. 2012; 13: 10305-15.

[42]

Leigh A, Zwieniecki MA, Rockwell FE et al. Structural and hydraulic correlates of heterophylly in Ginkgo biloba. New Phytol. 2011; 189: 459-70.

[43]

Bauer K, Grauvogel-Stamm L, Kustatscher E et al. Fossil ginkgophyte seedlings from the Triassic of France resemble modern Ginkgo biloba. BMC Evol Biol. 2013; 13: 177.

[44]

Ikeuchi M, Ogawa Y, Iwase A et al. Plant regeneration: cellular origins and molecular mechanisms. Development. 2016; 143: 1442-51.

[45]

Xu Z et al. Plant cell totipotency and regeneration. Sci Sin Vitae. 2019; 49: 1282-300.

[46]

Pijut PM, Woeste KE, Michler CH . Promotion of adventitious root formation of difficult-to-root hardwood tree species. Hortic Rev. 2011; 38: 213-51.

[47]

Zhou Z, Zheng S . Palaeobiology: the missing link in Ginkgo evolution. Nature. 2003; 423: 821-2.

[48]

Mathan J, Bhattacharya J, Ranjan A . Enhancing crop yield by optimizing plant developmental features. Development. 2016; 143: 3283-94.

[49]

Meyer RS, Purugganan MD . Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet. 2013; 14: 840-52.

[50]

Long SP, Zhu X, Naidu SL et al. Can improvement in photosynthesis increase crop yields. Plant Cell Environ. 2006; 29: 315-30.

[51]

Zhang T-Q, Lian H, Zhou C-M et al. Two-step model for de novo activation of WUSCHEL during plant shoot regeneration. Plant Cell. 2017; 29: 1073-87.

[52]

Wang J, Tian C, Zhang C et al. Cytokinin signaling activates WUSCHEL expression during axillary meristem initiation. Plant Cell. 2017; 29: 1373-87.

[53]

Liu H, Gao Y, Song X et al. A novel rejuvenation approach to induce endohormones and improve rhizogenesis in mature Juglans tree. Plant Methods. 2018; 14: 1-14.

[54]

Guan L, Murphy AS, Peer WA et al. Physiological and molecular regulation of adventitious root formation. Crit Rev Plant Sci. 2015; 34: 506-21.

[55]

Lucas WJ . Plant vascular biology and agriculture. J Integr Plant Biol. 2010; 52: 4-7.

[56]

Peer KR, Greenwood MS . Maturation, topophysis and other factors in relation to rooting in Larix. Tree Physiol. 2001; 21: 267-72.

[57]

Yang C-Q, Fang X, Wu X-M et al. Transcriptional regulation of plant secondary metabolism. J Integr Plant Biol. 2012; 54: 703-12.

[58]

Loreti E, Povero G, Novi G et al. Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol. 2008; 179: 1004-16.

[59]

Ji X-H, Wang Y-T, Zhang R et al. Effect of auxin, cytokinin and nitrogen on anthocyanin biosynthesis in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant Cell Tissue Organ Cult. 2015; 120: 325-37.

[60]

Lewis DR, Ramirez MV, Miller ND et al. Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiol. 2011; 156: 144-64.

[61]

Tan H, Man C, Xie Y et al. A crucial role of GA-regulated flavonol biosynthesis in root growth of Arabidopsis. Mol Plant. 2019; 12: 521-37.

[62]

Qiao X, Jiang S, Li X et al. Effects of phytohormones on plant regeneration and production of flavonoids in transgenic Saussurea involucrata hairy roots. Chine J Biotech. 2011; 27: 69-75.

[63]

Cheng C, Jiao C, Singer SD et al. Gibberellin-induced changes in the transcriptome of grapevine (Vitis labrusca × V. vinifera) cv. Kyoho flowers. Genomics. 2015; 16: 128.

[64]

Greenwood MS, Day ME, Schatz J . Separating the effects of tree size and meristem maturation on shoot development of grafted scions of red spruce (Picea rubens Sarg.). Tree Physiol. 2010; 30: 459-68.

[65]

Lu Z, Xu J, Li W et al. Transcriptomic analysis reveals mechanisms of sterile and fertile flower differentiation and development in Viburnum macrocephalum f. keteleeri. Front Plant Sci. 2017; 8: 261.

[66]

Pan X, Welti R, Wang X . Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc. 2010; 5: 986-92.

[67]

Wang L, Cui J, Jin B et al. Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees. Proc Natl Acad Sci U S A. 2020; 117: 2201-10.

[68]

Chen W, Gong L, Guo Z et al. A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites, application in the study of rice metabolomics. Mol Plant. 2013; 6: 1769-80.

[69]

Li W-X, Yang S-B, Lu Z et al. Cytological, physiological, and transcriptomic analyses of golden leaf coloration in Ginkgo biloba L. Hortic Res. 2018; 5: 12.

[70]

Kim D, Pertea G, Trapnell C et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14: R36.

[71]

Robinson MD, McCarthy DJ, Smyth GK . edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26: 139-40.

[72]

Chen C, Chen H, Zhang Y et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13: 1194-202.

PDF (3672KB)

59

Accesses

0

Citation

Detail

Sections
Recommended

/