Skip to main content

The role of plant hormones in tree-ring formation

Abstract

Key message

The spatial and temporal distributions of plant hormones during tree-ring formation are beginning to be elucidated. Plant hormones play specific roles in tree-ring formation depending on the developmental zone in which they operate.

Abstract

Tree rings are the result of the seasonal activity of the vascular cambium, the secondary meristem of woody angiosperms and gymnosperms. During tree-ring formation, a combination of endogenous and environmental factors affects cambial division, cell differentiation and maturation; this, in turn, affects wood quantity and quality. Among the endogenous factors affecting tree-ring formation, plant hormones are recognized as determinant players in regulating many aspects of the features and fate of each xylem cell. Most of our knowledge regarding the roles of plant hormones on tree-ring formation comes from herbaceous plants, although an increasing interest involves the analysis of the hormonal patterns in tree-species. This paper reviews the state of knowledge of the role of plant hormones during tree-ring formation by focusing on experiments performed on woody species. An overview of the main plant hormones and their main activities during radial tree growth will be followed by discussion of their role in each tree-ring developmental stage and in the overall tree-ring seasonal pattern.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Achard P, Cheng H, De Grauwe L et al (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  CAS  PubMed  Google Scholar 

  • Agusti J, Herold S, Schwarz M et al (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci 108:20242–20247

    Article  PubMed  PubMed Central  Google Scholar 

  • Ahmed S, Ariyaratne M, Patel J et al (2017) Altered expression of polyamine transporters reveals a role for spermidine in the timing of flowering and other developmental response pathways. Plant Sci 258:146–155

    Article  CAS  PubMed  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824

    Article  CAS  PubMed  Google Scholar 

  • Aloni R (2001) Foliar and axial aspects of vascular differentiation: hypotheses and evidence. J Plant Growth Regul 20:22–34. https://doi.org/10.1007/s003440010001

    Article  CAS  Google Scholar 

  • Aloni R (2007) Phytohormonal mechanisms that control wood quality formation in young and mature trees. In: The compromised wood workshop, pp 1–22

  • Aloni R (2013) Role of hormones in controlling vascular differentiation and the mechanism of lateral root initiation. Planta 238:819–830. https://doi.org/10.1007/s00425-013-1927-8

    Article  CAS  PubMed  Google Scholar 

  • Aloni R (2015) Ecophysiological implications of vascular differentiation and plant evolution. Trees 29:1–16

    Article  Google Scholar 

  • Aloni R, Tollier MT, Monties B (1990) The role of auxin and gibberellin in controlling lignin formation in primary phloem fibers and in xylem of Coleus blumei stems. Plant Physiol 94:1743–1747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aloni R, Langhans M, Aloni E et al (2005) Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56:1535–1544

    Article  CAS  PubMed  Google Scholar 

  • Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of auxin in regulating Arabidopsis flower development. Planta 223:315–328

    Article  CAS  PubMed  Google Scholar 

  • Alvim R, Hewett EW, Saunders PF (1976) Seasonal variation in the hormone content of Willow: I. Changes in abscisic acid content and cytokinin activity in the xylem Sap 1. Plant Physiol 57:474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arend M, Fromm J (2013) Concomitant analysis of cambial abscisic acid and cambial growth activity in poplar. Trees Struct Funct 27:1271–1276. https://doi.org/10.1007/s00468-013-0875-z

    Article  CAS  Google Scholar 

  • Baba K, Karlberg A, Schmidt J et al (2011) Activity–dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen. Proc Natl Acad Sci USA 108:3418–3423

    Article  PubMed  PubMed Central  Google Scholar 

  • Bai M-Y, Shang J-X, Oh E et al (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817. https://doi.org/10.1038/ncb2546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai W-Q, Xiao Y-H, Zhao J et al (2014) Gibberellin overproduction promotes sucrose synthase expression and secondary cell wall deposition in cotton fibers. PLoS One 9:e96537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bajguz A, Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62:1027–1046

    Article  CAS  PubMed  Google Scholar 

  • Balducci L, Cuny HE, Rathgeber CBK et al (2016) Compensatory mechanisms mitigate the effect of warming and drought on wood formation. Plant Cell Environ 39:1338–1352. https://doi.org/10.1111/pce.12689

    Article  CAS  PubMed  Google Scholar 

  • Barlow P (2005) From cambium to early cell differentiation within the secondary vascular system. In: Vascular transport in plants. Elsevier, pp 279–306

  • Barra-Jiménez A, Ragni L (2017) Secondary development in the stem: when Arabidopsis and trees are closer than it seems. Curr Opin Plant Biol 35:145–151. https://doi.org/10.1016/j.pbi.2016.12.002

    Article  PubMed  Google Scholar 

  • Beeckman H (2016) Wood anatomy and trait-based ecology. IAWA J 37:127–151

    Article  Google Scholar 

  • Begum S, Kudo K, Rahman MH et al (2018) Climate change and the regulation of wood formation in trees by temperature. Trees. https://doi.org/10.1007/s00468-017-1587-6

    Article  Google Scholar 

  • Bennett T, Hines G, Leyser O (2014) Canalization: what the flux? Trends Genet 30:41–48

    Article  CAS  PubMed  Google Scholar 

  • Bhalerao RP, Fischer U (2014) Auxin gradients across wood—instructive or incidental? Physiol Plant 151:43–51

    Article  CAS  PubMed  Google Scholar 

  • Bhalerao RP, Fischer U (2016) Environmental and hormonal control of cambial stem cell dynamics. J Exp Bot 68:79–87

    Article  CAS  PubMed  Google Scholar 

  • Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135:254–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bishopp A, Lehesranta S, Vatén A et al (2011) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21:927–932

    Article  CAS  PubMed  Google Scholar 

  • Björklund S, Antti H, Uddestrand I et al (2007) Cross-talk between gibberellin and auxin in development of Populus wood: gibberellin stimulates polar auxin transport and has a common transcriptome with auxin. Plant J 52:499–511. https://doi.org/10.1111/j.1365-313X.2007.03250.x

    Article  CAS  PubMed  Google Scholar 

  • Björklund J, Seftigen K, Schweingruber F et al (2017) Cell size and wall dimensions drive distinct variability of earlywood and latewood density in Northern Hemisphere conifers. New Phytol 216:728–740

    Article  CAS  PubMed  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  CAS  PubMed  Google Scholar 

  • Bossinger G, Spokevicius AV (2018) Sector analysis reveals patterns of cambium differentiation in poplar stems. J Exp Bot 69:4339–4348. https://doi.org/10.1093/jxb/ery230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford KJ, Yang SF (1980) Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants. Plant Physiol 65:322–326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brumos J, Robles LM, Yun J et al (2018) Local auxin biosynthesis is a key regulator of plant development. Dev Cell 47:306–318.e5. https://doi.org/10.1016/j.devcel.2018.09.022

    Article  CAS  PubMed  Google Scholar 

  • Brunner AM, Nilsson O (2004) Revisiting tree maturation and floral initiation in the poplar functional genomics era. New Phytol 164:43–51

    Article  CAS  PubMed  Google Scholar 

  • Cai G, Sobieszczuk-Nowicka E, Aloisi I et al (2015) Polyamines are common players in different facets of plant programmed cell death. Amino Acids 47:27–44

    Article  CAS  PubMed  Google Scholar 

  • Cartenì F, Deslauriers A, Rossi S et al (2018) The physiological mechanisms behind the earlywood-to-latewood transition: a process-based modelling approach. Front Plant Sci 9:1053

    Article  PubMed  PubMed Central  Google Scholar 

  • Cecchetti V, Altamura MM, Brunetti P et al (2013) Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. Plant J 74:411–422

    Article  CAS  PubMed  Google Scholar 

  • Chaffey N (1999) Wood formation in forest trees: from Arabidopsis to Zinnia. Trends Plant Sci 4:203–204

    Article  CAS  PubMed  Google Scholar 

  • Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol Plant 114:594–600

    Article  CAS  PubMed  Google Scholar 

  • Chaffey PK, Guan X, Wang L-X, Tan Z (2017) Introduction: general aspects of the chemical biology of glycoproteins In: Wang L-X, Tan Z (eds) Chemical Biology of Glycoproteins, Royal Society of Chemistry, pp 1–19

  • Chen D, Shao Q, Yin L et al (2018) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01945

    Article  PubMed  PubMed Central  Google Scholar 

  • Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Biol 49:427–451

    Article  CAS  Google Scholar 

  • Coleman HD, Samuels AL, Guy RD, Mansfield SD (2008) Perturbed lignification impacts tree growth in hybrid poplar—a function of sink strength, vascular integrity, and photosynthetic assimilation. Plant Physiol 148:1229–1237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cook CE, Whichard LP, Turner B et al (1966) Germination of witchweed (striga lutea lour.): Isolation and properties of a potent stimulant. Sci 154:1189–1190. https://doi.org/10.1126/science.154.3753.1189

    Article  CAS  Google Scholar 

  • Cook CM, Daudi A, Millar DJ et al (2012) Transcriptional changes related to secondary wall formation in xylem of transgenic lines of tobacco altered for lignin or xylan content which show improved saccharification. Phytochemistry 74:79–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuny HE, Rathgeber CBKK (2016) Xylogenesis: coniferous trees of temperate forests are listening to the climate tale during the growing season but only remember the last words! Plant Physiol 171:306–317. https://doi.org/10.1104/pp.16.00037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuny HE, Rathgeber CBKBK, Frank D et al (2014) Kinetics of tracheid development explain conifer tree-ring structure. New Phytol 203:1231–1241. https://doi.org/10.1111/nph.12871

    Article  PubMed  Google Scholar 

  • Cutler AJ, Krochko JE (1999) Formation and breakdown of ABA. Trends Plant Sci 4:472–478

    Article  CAS  PubMed  Google Scholar 

  • Davies PJ (2010) The plant hormones: their nature, occurrence, and functions. Plant hormones. Springer Netherlands, Dordrecht, pp 1–15

    Chapter  Google Scholar 

  • De Rybel B, Adibi M, Breda AS et al (2014) Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science 345:1255215

    Article  CAS  PubMed  Google Scholar 

  • Dello Ioio R, Nakamura K, Moubayidin L et al (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384

    Article  CAS  PubMed  Google Scholar 

  • Delpierre N, Lireux S, Hartig F et al (2019) Chilling and forcing temperatures interact to predict the onset of wood formation in Northern Hemisphere conifers. Glob Chang Biol 25:1089–1105

    PubMed  Google Scholar 

  • Denne MP (1989) Definition of latewood according to Mork (1928). IAWA J 10:59–62. https://doi.org/10.1163/22941932-90001112

    Article  Google Scholar 

  • Deslauriers A, Huang J-G, Balducci L et al (2016) The contribution of carbon and water in modulating wood formation in black spruce saplings. Plant Physiol 170:2072–2084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dewitte W, Scofield S, Alcasabas AA et al (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci 104:14537–14542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Didi V, Jackson P, Hejátko J (2015) Hormonal regulation of secondary cell wall formation. J Exp Bot 66:5015–5027. https://doi.org/10.1093/jxb/erv222

    Article  CAS  PubMed  Google Scholar 

  • Dobrev PI, Kamı́nek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950:21–29

    Article  PubMed  Google Scholar 

  • Dodd IC (2003) Hormonal interactions and stomatal responses. J Plant Growth Regul 22:32–46. https://doi.org/10.1007/s00344-003-0023-x

    Article  CAS  Google Scholar 

  • Dodd IC, Davies WJ (2010) Hormones and the regulation of water balance. Plant Hormones. Springer Netherlands, Dordrecht, pp 519–548

    Chapter  Google Scholar 

  • Douglass AE (1919) Climatic cycles and tree growth: a study of the annual rings of trees in relation to climated and solar activity. Carnegie Institution of Washington, Washington

    Book  Google Scholar 

  • Downes GM, Wimmer R, Evans R (2002) Understanding wood formation: gains to commercial forestry through tree-ring research. Dendrochronologia 20:37–51

    Article  Google Scholar 

  • Druart N, Johansson A, Baba K et al (2007) Environmental and hormonal regulation of the activity–dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks. Plant J 50:557–573

    Article  CAS  PubMed  Google Scholar 

  • Du S, Yamamoto F (2007) An overview of the biology of reaction wood formation. J Integr Plant Biol 49:131–143

    Article  CAS  Google Scholar 

  • Dünser K, Kleine-Vehn J (2015) Differential growth regulation in plants—the acid growth balloon theory. Curr Opin Plant Biol 28:55–59

    Article  CAS  PubMed  Google Scholar 

  • Edlund A, Eklof S, Sundberg B et al (1995) A microscale technique for gas chromatography-mass spectrometry measurements of picogram amounts of indole-3-acetic acid in plant tissues. Plant Physiol 108:1043–1047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eklund L (1993) Movement and possible metabolism of ethylene in dormant Picea abies. Plant Growth Regul 12:37–41

    Article  CAS  Google Scholar 

  • Emery RJN, Ma Q, Atkins CA (2000) The forms and sources of cytokinins in developing white lupine seeds and fruits. Plant Physiol 123:1593–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson ME, Moritz T (2002) Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen (Populus tremula L. × P. tremuloides Michx.). Planta 214:920–930

    Article  CAS  PubMed  Google Scholar 

  • Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788

    Article  CAS  PubMed  Google Scholar 

  • Espinosa-Ruiz A, Saxena S, Schmidt J et al (2004) Differential stage-specific regulation of cyclin-dependent kinases during cambial dormancy in hybrid aspen. Plant J 38:603–615

    Article  CAS  PubMed  Google Scholar 

  • Fajstavr M, Paschová Z, Giagli K et al (2018) Auxin (IAA) and soluble carbohydrate seasonal dynamics monitored during xylogenesis and phloemogenesis in Scots pine. iForest-Biogeosciences For 11:553

    Article  Google Scholar 

  • Falcioni R, Moriwaki T, de Oliveira DM et al (2018) Increased gibberellins and light levels promotes cell wall thickness and enhance lignin deposition in xylem fibers. Front Plant Sci 9:1–13. https://doi.org/10.3389/fpls.2018.01391

    Article  Google Scholar 

  • Fäldt J, Martin D, Miller B et al (2003) Traumatic resin defense in Norway spruce (Picea abies): methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Mol Biol 51:119–133

    Article  PubMed  Google Scholar 

  • Fath A, Bethke P, Lonsdale J et al (2000) Programmed cell death in cereal aleurone. Plant Mol Biol 44:255–266

    Article  CAS  PubMed  Google Scholar 

  • Fath A, Bethke PC, Jones RL (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felten J, Vahala J, Love J et al (2018) Ethylene signaling induces gelatinous layers with typical features of tension wood in hybrid aspen. New Phytol 218:999–1014. https://doi.org/10.1111/nph.15078

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein R (2013) Abscisic acid synthesis and response. Arab book/American Soc Plant Biol 11:e0166

    Google Scholar 

  • Fonti P, Von Arx G, García-González I et al (2010) Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytol 185:42–53. https://doi.org/10.1111/j.1469-8137.2009.03030.x

    Article  PubMed  Google Scholar 

  • Franceschini T, Martin-Ducup O, Schneider R (2016) Allometric exponents as a tool to study the influence of climate on the trade-off between primary and secondary growth in major north-eastern American tree species. Ann Bot 117:551–563. https://doi.org/10.1093/aob/mcw003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritts H (2012) Tree rings and climate. Academic Press, London

    Google Scholar 

  • Fromm J (1997) Hormonal physiology of wood growth in willow (Salix viminalis L.): effects of spermine and abscisic acid. Wood Sci Technol 31:119–130

    CAS  Google Scholar 

  • Funada R, Sugiyama T, Kubo T, Fushitani M (1988) Determination of abscisic acid in pinus densiflora by selected ion monitoring. Plant Physiol 88:525–527. https://doi.org/10.1104/pp.88.3.525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Funada R, Kubo T, Tabuchi M et al (2001) Seasonal variations in endogenous indole-3-acetic acid and abscisic acid in the cambial region of Pinus densiflora Sieb. et Zucc. Stems in relation to earlywood-latewood transition and cessation of tracheid production. Holzforschung 55:128–134. https://doi.org/10.1515/HF.2001.021

    Article  CAS  Google Scholar 

  • Funada R, Kubo T, Sugiyama T, Fushitani M (2002) Changes in levels of endogenous plant hormones in cambial regions of stems of Larix kaempferi at the onset of cambial activity in springtime. J Wood Sci 48:75

    Article  CAS  Google Scholar 

  • Funada R, Miura T, Shimizu Y et al (2008) Gibberellin-induced formation of tension wood in angiosperm trees. Planta 227:1409–1414

    Article  CAS  PubMed  Google Scholar 

  • Funada R, Yamagishi Y, Begum S et al (2016) Xylogenesis in trees: from cambial cell division to cell death. In: Secondary xylem biology. Elsevier, pp 25–43

  • Galston AW, Sawhney RK (1990) Polyamines in plant physiology. Plant Physiol 94:406–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270:1986–1988

    Article  CAS  PubMed  Google Scholar 

  • Giannarelli S, Muscatello B, Bogani P et al (2010) Comparative determination of some phytohormones in wild-type and genetically modified plants by gas chromatography–mass spectrometry and high-performance liquid chromatography–tandem mass spectrometry. Anal Biochem 398:60–68

    Article  CAS  PubMed  Google Scholar 

  • Grichko VP, Glick BR (2001) Ethylene and flooding stress in plants. Plant Physiol Biochem 39:1–9

    Article  CAS  Google Scholar 

  • Grove MD, Spencer GF, Rohwedder WK et al (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281:216

    Article  CAS  Google Scholar 

  • Gu B, Zhou T, Luo J et al (2015) An-2 encodes a cytokinin synthesis enzyme that regulates awn length and grain production in rice. Mol Plant 8:1635–1650

    Article  CAS  PubMed  Google Scholar 

  • Guerriero G, Hausman J-F, Cai G (2014) No stress! Relax! Mechanisms governing growth and shape in plant cells. Int J Mol Sci 15:5094–5114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo J, Kwon H-K, Wang M-H (2010) Characterization of three A-type cyclin genes in tomato (Solanum lycopersicum) treated with auxins. J Korean Soc Appl Biol Chem 53:266–274

    Article  CAS  Google Scholar 

  • Gusta LV, Trischuk R, Weiser CJ (2005) Plant cold acclimation: the role of abscisic acid. J Plant Growth Regul 24:308–318

    Article  CAS  Google Scholar 

  • Hacke UG, Spicer R, Schreiber SG, Plavcová L (2017) An ecophysiological and developmental perspective on variation in vessel diameter. Plant Cell Environ 40:831–845. https://doi.org/10.1111/pce.12777

    Article  CAS  PubMed  Google Scholar 

  • Harashima H, Kato K, Shinmyo A, Sekine M (2007) Auxin is required for the assembly of A-type cyclin-dependent kinase complexes in tobacco cell suspension culture. J Plant Physiol 164:1103–1112

    Article  CAS  PubMed  Google Scholar 

  • Hartmann FP, Rathgeber CBK, Fournier M, Moulia B (2017) Modelling wood formation and structure: power and limits of a morphogenetic gradient in controlling xylem cell proliferation and growth. Ann For Sci 74:14

    Article  Google Scholar 

  • He Y, Li J, Ban Q et al (2018) Role of brassinosteroids in persimmon (Diospyros kaki L.) fruit ripening. J Agric Food Chem 66:2637–2644

    Article  CAS  PubMed  Google Scholar 

  • Hedden P (2016) Annual plant reviews, the gibberellins. Wiley, New York

    Book  Google Scholar 

  • Hellgren JM, Olofsson K, Sundberg B (2004) Patterns of auxin distribution during gravitational induction of reaction wood in poplar and pine. Plant Physiol 135:212–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirose N, Takei K, Kuroha T et al (2007) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59:75–83

    Article  CAS  PubMed  Google Scholar 

  • Hossain Z, McGarvey B, Amyot L et al (2012) DIMINUTO 1 affects the lignin profile and secondary cell wall formation in Arabidopsis. Planta 235:485–498

    Article  CAS  PubMed  Google Scholar 

  • Howell SH, Lall S, Che P (2003) Cytokinins and shoot development. Trends Plant Sci 8:453–459

    Article  CAS  PubMed  Google Scholar 

  • Hudgins JW, Franceschi VR (2004) Methyl jasmonate-induced ethylene production is responsible for conifer phloem defense responses and reprogramming of stem cambial zone for traumatic resin duct formation. Plant Physiol 135:2134–2149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hudgins JW, Christiansen E, Franceschi VR (2004) Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: a phylogenetic perspective. Tree Physiol 24:251–264

    Article  CAS  PubMed  Google Scholar 

  • Hudgins JW, Ralph SG, Franceschi VR, Bohlmann J (2006) Ethylene in induced conifer defense: cDNA cloning, protein expression, and cellular and subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in resin duct and phenolic parenchyma cells. Planta 224:865–877. https://doi.org/10.1007/s00425-006-0274-4

    Article  CAS  PubMed  Google Scholar 

  • Iakimova ET, Woltering EJ (2017) Xylogenesis in zinnia (Zinnia elegans) cell cultures: unravelling the regulatory steps in a complex developmental programmed cell death event. Planta 245:681–705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Immanen J, Nieminen K, Smolander OP et al (2016) Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr Biol 26:1990–1997. https://doi.org/10.1016/j.cub.2016.05.053

    Article  CAS  PubMed  Google Scholar 

  • Ingemarsson BSM, Eklund L, Eliasson L (1991a) Ethylene effects on cambial activity and cell wall formation in hypocotyls of Picea abies seedlings. Physiol Plant 82:219–224

    Article  CAS  Google Scholar 

  • Ingemarsson BSM, Lundqvist E, Eliasson L (1991b) Seasonal variation in ethylene concentration in the wood of Pinus sylvestris L. Tree Physiol 8:273–279

    Article  CAS  PubMed  Google Scholar 

  • Irving RM, Lanphear FO (1968) Regulation of cold hardiness in Acer negundo. Plant Physiol 43:9–13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Israelsson M, Sundberg B, Moritz T (2005) Tissue-specific localization of gibberellins and expression of gibberellin-biosynthetic and signaling genes in wood-forming tissues in aspen. Plant J 44:494–504. https://doi.org/10.1111/j.1365-313X.2005.02547.x

    Article  CAS  PubMed  Google Scholar 

  • Ivakov A, Persson S (2012) Plant cell walls. eLS. Wiley, New York

    Google Scholar 

  • Jackson M (1997) Hormones from roots as signals for the shoots of stressed plants. Trends Plant Sci 2:22–28

    Article  Google Scholar 

  • Jeon HW, Cho JS, Park EJ et al (2016) Developing xylem-preferential expression of PdGA20ox1, a gibberellin 20-oxidase 1 from Pinus densiflora, improves woody biomass production in a hybrid poplar. Plant Biotechnol J 14:1161–1170. https://doi.org/10.1111/pbi.12484

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Do J, Shin SJ et al (2014) Exogenously applied 24-epi brassinolide reduces lignification and alters cell wall carbohydrate biosynthesis in the secondary xylem of Liriodendron tulipifera. Phytochemistry 101:40–51. https://doi.org/10.1016/j.phytochem.2014.02.003

    Article  CAS  PubMed  Google Scholar 

  • Jiroutova P, Oklestkova J, Strnad M (2018) Crosstalk between brassinosteroids and ethylene during plant growth and under abiotic stress conditions. Int J Mol Sci 19:3283

    Article  CAS  PubMed Central  Google Scholar 

  • Johnson D, Eckart P, Alsamadisi N et al (2018) Polar auxin transport is implicated in vessel differentiation and spatial patterning during secondary growth in Populus. Am J Bot 105:186–196

    Article  CAS  PubMed  Google Scholar 

  • Johnsson C, Jin X, Xue W et al (2019) The plant hormone auxin directs timing of xylem development by inhibition of secondary cell wall deposition through repression of secondary wall NAC-domain transcription factors. Physiol Plant 165:673–689

    Article  CAS  PubMed  Google Scholar 

  • Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125:94–97. https://doi.org/10.1104/pp.125.1.94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Junghans U, Langenfeld-Heyser R, Polle A, Teichmann T (2004) Effect of auxin transport inhibitors and ethylene on the wood anatomy of poplar. Plant Biol 6:22–29. https://doi.org/10.1055/s-2003-44712

    Article  CAS  PubMed  Google Scholar 

  • Kalev N, Aloni R (1999) Role of ethylene and auxin in regenerative differentiation and orientation of tracheids in Pinus pinea seedlings. New Phytol 142:307–313

    Article  CAS  Google Scholar 

  • Kaneda M, Rensing K, Samuels L (2010) Secondary cell wall deposition in developing secondary xylem of poplar. J Integr Plant Biol 52:234–243. https://doi.org/10.1111/j.1744-7909.2010.00925.x

    Article  CAS  PubMed  Google Scholar 

  • Kaneko M, Itoh H, Inukai Y et al (2003) Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J 35:104–115

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Lee Y, Sakakibara H, Martinoia E (2017a) Cytokinin transporters: GO and STOP in signaling. Trends Plant Sci 22:455–461. https://doi.org/10.1016/j.tplants.2017.03.003

    Article  CAS  PubMed  Google Scholar 

  • Kang YH, Breda A, Hardtke CS (2017b) Brassinosteroid signaling directs formative cell divisions and protophloem differentiation in Arabidopsis root meristems. Development 144:272–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karpaga Raja Sundari B, Ghosh Dasgupta M (2014) Isolation of developing secondary xylem specific cellulose synthase genes and their expression profiles during hormone signalling in Eucalyptus tereticornis. J Genet 93:403–414. https://doi.org/10.1007/s12041-014-0391-y

    Article  CAS  Google Scholar 

  • Kim S-K, Abe H, Little CHA et al (1990) Identification of two brassinosteroids from the cambial region of Scots pine (Pinus sylvestris) by gas chromatography-mass spectrometry, after detection using a dwarf rice lamina inclination bioassay. Plant Physiol 94:1709–1713. https://doi.org/10.1104/pp.94.4.1709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klintborg A, Eklund L, Little CHA (2002) Ethylene metabolism in scots pine (Pinus sylvestris) shoots during the year. Tree Physiol 22:59–66

    Article  CAS  PubMed  Google Scholar 

  • Kotov AA, Kotova LM (2000) The contents of auxins and cytokinins in pea internodes as related to the growth of lateral buds. J Plant Physiol 156:438–448

    Article  CAS  Google Scholar 

  • Křeček P, Skůpa P, Libus J et al (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krokene P, Nagy NE, Solheim H (2008) Methyl jasmonate and oxalic acid treatment of Norway spruce: anatomically based defense responses and increased resistance against fungal infection. Tree Physiol 28:29–35. https://doi.org/10.1093/treephys/28.1.29

    Article  CAS  PubMed  Google Scholar 

  • Kubo M, Udagawa M, Nishikubo N et al (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar M, Campbell L, Turner S (2015) Secondary cell walls: biosynthesis and manipulation. J Exp Bot 67:515–531

    Article  CAS  PubMed  Google Scholar 

  • Kuriyama H, Fukuda H (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5:568–573

    Article  CAS  PubMed  Google Scholar 

  • Kuroha T, Tokunaga H, Kojima M et al (2009) Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21:3152–3169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lachaud S (1989) Participation of auxin and abscisic acid in the regulation of seasonal variations in cambial activity and xylogenesis. Trees 3:125–137

    Article  Google Scholar 

  • Lachaud S, Catesson A-M, Bonnemain J-L (1999) Structure and functions of the vascular cambium. Comptes Rendus l’Académie des Sci Ser III Sci la Vie 322:633–650. https://doi.org/10.1016/S0764-4469(99)80103-6

    Article  CAS  Google Scholar 

  • Larson PR (1960) A physiological consideration of the springwood summerwood transition in Red Pine [Pinus resinosa]. For Sci 6:110–122

    CAS  Google Scholar 

  • Larson PR (1969) Wood formation and the concept of wood quality. Bull no 74 New Haven. CT Yale Univ Sch For 54:1–54

    Google Scholar 

  • Larson PR (2012) The vascular cambium: development and structure. Springer Science and Business Media, New York

    Google Scholar 

  • Lee J, Han S, Lee H-Y et al (2019) Brassinosteroids facilitate xylem differentiation and wood formation in tomato. Planta 249:1391–1403. https://doi.org/10.1007/s00425-019-03094-6

    Article  CAS  PubMed  Google Scholar 

  • Letham DS (1994) Cytokinins as phytohormones—sites of biosynthesis, translocation, and function of translocated cytokinin. In: Mok DWS, Mok MC (eds) Cytokinins. Activity and function. CRC Press, Boca Raton, pp 57–80

    Google Scholar 

  • Leyser O (2005) Auxin distribution and plant pattern formation: how many angels can dance on the point of PIN? Cell 121:819–822

    Article  CAS  PubMed  Google Scholar 

  • Little CHA, Pharis RP (1995) Hormonal control of radial and longitudinal growth in the tree stem. In: Plant stems. Elsevier, pp 281–319

  • Little CHA, Savidge RA (1987) The role of plant growth regulators in forest tree cambial growth. Springer, Dordrecht, pp 137–169

    Google Scholar 

  • Little CHA, Wareing PF (1981) Control of cambial activity and dormancy in Picea sitchensis by indol-3-ylacetic and abscisic acids. Can J Bot 59:1480–1493

    Article  CAS  Google Scholar 

  • Liu M, Pirrello J, Chervin C et al (2015) Ethylene control of fruit ripening: revisiting the complex network of transcriptional regulation. Plant Physiol 169:2380–2390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu QY, Guo GS, Qiu ZF et al (2018) Exogenous GA3 application altered morphology, anatomic and transcriptional regulatory networks of hormones in Eucalyptus grandis. Protoplasma 255:1107–1119. https://doi.org/10.1007/s00709-018-1218-0

    Article  CAS  PubMed  Google Scholar 

  • Ljung K, Hull AK, Celenza J et al (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090–1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Locato V, De Gara L (2018) Programmed cell death in plants: an overview. In: Plant programmed cell death. Springer, pp 1–8

  • Löfke C, Dünser K, Scheming D, Kleine-Vehn J (2015) Auxin regulates SNARE-dependent vacuolar morphology restricting cell size. Elife. https://doi.org/10.7554/eLife.05868

    Article  PubMed  PubMed Central  Google Scholar 

  • Love J, Björklund S, Vahala J et al (2009) Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. Proc Natl Acad Sci 106:5984–5989

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma Y, Cao J, He J et al (2018) Molecular mechanism for the regulation of ABA homeostasis during plant development and stress responses. Int J Mol Sci 19:3643

    Article  CAS  PubMed Central  Google Scholar 

  • Majda M, Robert S (2018) The role of auxin in cell wall expansion. Int J Mol Sci 19:951

    Article  CAS  PubMed Central  Google Scholar 

  • Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129:1003–1018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martín JA, Solla A, García-Vallejo MC, Gil L (2012) Chemical changes in Ulmus minor xylem tissue after salicylic acid or carvacrol treatments are associated with enhanced resistance to Ophiostoma novo-ulmi. Phytochemistry 83:104–109. https://doi.org/10.1016/j.phytochem.2012.07.017

    Article  CAS  PubMed  Google Scholar 

  • Martin-Vertedor AI, Dodd IC (2011) Root-to-shoot signalling when soil moisture is heterogeneous: increasing the proportion of root biomass in drying soil inhibits leaf growth and increases leaf abscisic acid concentration. Plant Cell Environ 34:1164–1175. https://doi.org/10.1111/j.1365-3040.2011.02315.x

    Article  CAS  PubMed  Google Scholar 

  • McLean A, Smith JHG (1973) Effects of climate on forage yields and tree-ring widths in British Columbia. J Range Manag 26:416–419

    Article  Google Scholar 

  • McSteen P, Zhao Y (2008) Plant hormones and signaling: common themes and new developments. Dev Cell 14:467–473

    Article  CAS  PubMed  Google Scholar 

  • Meng F-R, Arp PA (1993) Net photosynthesis and stomatal conductance of red spruce twigs before and after twig detachment. Can J For Res 23:716–721. https://doi.org/10.1139/x93-093

    Article  Google Scholar 

  • Milborrow BV (2001) The pathway of biosynthesis of abscisic acid in vascular plants: a review of the present state of knowledge of ABA biosynthesis. J Exp Bot 52:1145–1164

    Article  CAS  PubMed  Google Scholar 

  • Milhinhos A, Miguel CM (2013) Hormone interactions in xylem development: a matter of signals. Plant Cell Rep 32:867–883. https://doi.org/10.1007/s00299-013-1420-7

    Article  CAS  PubMed  Google Scholar 

  • Milhinhos A, Prestele J, Bollhöner B et al (2013) Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem. Plant J 75:685–698

    Article  CAS  PubMed  Google Scholar 

  • Milioni D, Sado P-E, Stacey NJ et al (2001) Differential expression of cell-wall-related genes during the formation of tracheary elements in the Zinnia mesophyll cell system. Plant Mol Biol 47:221–238

    Article  CAS  PubMed  Google Scholar 

  • Miller RB (1999) Structure of wood. Wood handbook: wood as an engineering material. Madison, WI USDA For Serv For Prod Lab General te:2.1-2.4,113

  • Mitchum MG, Yamaguchi S, Hanada A et al (2006) Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J 45:804–818

    Article  CAS  PubMed  Google Scholar 

  • Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37:128–138

    Article  CAS  PubMed  Google Scholar 

  • Moritz T, Sundberg B (1996) Endogenous cytokinins in the vascular cambial region of Pinus sylvestris during activity and dormancy. Physiol Plant 98:693–698. https://doi.org/10.1111/j.1399-3054.1996.tb06673.x

    Article  CAS  Google Scholar 

  • Motose H, Iwamoto K, Endo S et al (2009) Involvement of phytosulfokine in the attenuation of stress response during the transdifferentiation of zinnia mesophyll cells into tracheary elements. Plant Physiol 150:437–447. https://doi.org/10.1104/pp.109.135954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moyle R, Schrader J, Stenberg A et al (2002) Environmental and auxin regulation of wood formation involves members of the Aux/IAA gene family in hybrid aspen. Plant J 31:675–685

    Article  CAS  PubMed  Google Scholar 

  • Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends Plant Sci 6:535–542

    Article  CAS  PubMed  Google Scholar 

  • Müller B, Sheen J (2008) Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:1094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mwange K-N, Hou H-W, Wang Y-Q et al (2005) Opposite patterns in the annual distribution and time-course of endogenous abscisic acid and indole-3-acetic acid in relation to the periodicity of cambial activity in Eucommia ulmoides Oliv. J Exp Bot 56:1017–1028

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Yamaguchi M, Endo H et al (2015) NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Front Plant Sci 6:288. https://doi.org/10.3389/fpls.2015.00288

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970

    Article  CAS  PubMed  Google Scholar 

  • Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:e258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475

    Article  CAS  PubMed  Google Scholar 

  • Nieminen K, Immanen J, Laxell M et al (2008) Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci 105:20032–20037. https://doi.org/10.1073/pnas.0805617106

    Article  PubMed  PubMed Central  Google Scholar 

  • Nilsson J, Karlberg A, Antti H et al (2008) Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell Online 20:843–855. https://doi.org/10.1105/tpc.107.055798

    Article  CAS  Google Scholar 

  • Novák O, Napier R, Ljung K (2017) Zooming in on plant hormone analysis: tissue-and cell-specific approaches. Annu Rev Plant Biol 68:323–348

    Article  CAS  PubMed  Google Scholar 

  • Nugroho WD, Nakaba S, Yamagishi Y et al (2013) Gibberellin mediates the development of gelatinous fibres in the tension wood of inclined Acacia mangium seedlings. Ann Bot 112:1321–1329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neill DP, Ross JJ (2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiol 130:1974–1982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Obroucheva NV (2008) Cell elongation as an inseparable component of growth in terrestrial plants. Russ J Dev Biol 39:13–24

    Article  Google Scholar 

  • Oda Y, Mimura T, Hasezawa S (2005) Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol 137:1027–1036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y et al (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oribe Y, Funada R, Kubo T (2003) Relationships between cambial activity, cell differentiation and the localization of starch in storage tissues around the cambium in locally heated stems of Abies sachalinensis (Schmidt) Masters. Trees 17:185–192

    Article  Google Scholar 

  • Osugi A, Sakakibara H (2015) Q&A: how do plants respond to cytokinins and what is their importance? BMC Biol 13:102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paponov IA, Teale WD, Trebar M et al (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10:170–177

    Article  CAS  PubMed  Google Scholar 

  • Park Y-ID, Spiecker H (2005) Variations in the tree-ring structure of Norway spruce (Picea abies) under contrasting climates. Dendrochronologia 23:93–104

    Article  Google Scholar 

  • Pesquet E, Tuominen H (2011) Ethylene stimulates tracheary element differentiation in Zinnia elegans cell cultures. New Phytol 190:138–149

    Article  CAS  PubMed  Google Scholar 

  • Pesquet E, Zhang B, Gorzsás A et al (2013) Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell 25:1314–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688

    Article  CAS  PubMed  Google Scholar 

  • Pharis RP, Jenkins PA, Aoki H, Sassa T (1981) Hormonal physiology of wood growth in Pinus radiata D. Don: effects of gibberellin A4 and the influence of abscisic acid upon (3H) gibberellin A4 metabolism. Funct Plant Biol 8:559–570

    Article  CAS  Google Scholar 

  • Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees wood formation in trees. Plant Physiol 127:1513–1523. https://doi.org/10.1104/pp.010816.1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prinsen E, Van Dongen W, Esmans EL, Van Onckelen HA (1998) Micro and capillary liquid chromatography–tandem mass spectrometry: a new dimension in phytohormone research. J Chromatogr A 826:25–37

    Article  CAS  Google Scholar 

  • Rahman MH, Begum S, Nakaba S et al (2016) Relationship between the earlywood-to-latewood transition and changes in levels of stored starch around the cambium in locally heated stems of the evergreen conifer Chamaecyparis pisifera. Trees 30:1619–1631

    Article  CAS  Google Scholar 

  • Rao X, Dixon RA (2017) Brassinosteroid mediated cell wall remodeling in grasses under abiotic stress. Front Plant Sci 8:806

    Article  PubMed  PubMed Central  Google Scholar 

  • Rayle DL, Cleland RE (1992) The Acid Growth Theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reisen D, Leborgne-Castel N, Özalp C et al (2003) Expression of a cauliflower tonoplast aquaporin tagged with GFP in tobacco suspension cells correlates with an increase in cell size. Plant Mol Biol 52:387–400

    Article  CAS  PubMed  Google Scholar 

  • Resman L, Howe G, Jonsen D et al (2010) Components acting downstream of SD perception regulate differential cessation of cambial activity and associated responses in early and late clones of hybrid poplar. Plant Physiol 154:1294–1303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richard C, Lescot M, Inzé D, De Veylder L (2002) Effect of auxin, cytokinin, and sucrose on cell cycle gene expression in Arabidopsis thaliana cell suspension cultures. Plant Cell Tissue Organ Cult 69:167–176

    Article  CAS  Google Scholar 

  • Ridoutt BG, Pharis RP, Sands R (1996) Fibre length and gibberellins A1 and A20 are decreased in Eucalyptus globulus by acylcyclohexanedione injected into the stem. Physiol Plant 96:559–566

    Article  CAS  Google Scholar 

  • Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544

    Article  CAS  PubMed  Google Scholar 

  • Ross JJ, Quittenden LJ (2016) Interactions between brassinosteroids and gibberellins: synthesis or Signaling? Plant Cell 28:829–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rossi S, Deslauriers A, Anfodillo T et al (2006) Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytol 170:301–310. https://doi.org/10.1111/j.1469-8137.2006.01660.x

    Article  PubMed  Google Scholar 

  • Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007) Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152:1–12. https://doi.org/10.1007/s00442-006-0625-7

    Article  PubMed  Google Scholar 

  • Samuels A, Rensing K, Douglas C et al (2002) Cellular machinery of wood production: differentiation of secondary xylem in Pinus contorta var. latifolia. Planta 216:72–82. https://doi.org/10.1007/s00425-002-0884-4

    Article  CAS  PubMed  Google Scholar 

  • Savada RP, Ozga JA, Jayasinghege CPA et al (2017) Heat stress differentially modifies ethylene biosynthesis and signaling in pea floral and fruit tissues. Plant Mol Biol 95:313–331

    Article  CAS  PubMed  Google Scholar 

  • Savidge RA (1988) Auxin and ethylene regulation of diameter growth in trees. Tree Physiol 4:401–414

    Article  CAS  PubMed  Google Scholar 

  • Savidge RA (1991) Seasonal cambial activity in Larix laricina saplings in relation to endogenous indol-3-ylacetic acid, sucrose, and coniferin. For Sci 37:953–958

    Google Scholar 

  • Savidge R (2001) Intrinsic regulation of cambial growth. J Plant Growth Regul 20:52–77

    Article  CAS  Google Scholar 

  • Savidge R, Wareing P (1984) Seasonal cambial activity and xylem development in Pinus contorta in relation to endogenous indol-3-yl-acetic and (S)-abscisic acid levels. Can J For Res 14:676–682

    Article  CAS  Google Scholar 

  • Savidge RA, Heald JK, Wareing PF (1982) Non-uniform distribution and seasonal variation of endogenous indol-3yl-acetic acid in the cambial region of Pinus contorta Dougl. Planta 155:89–92. https://doi.org/10.1007/BF00402937

    Article  CAS  PubMed  Google Scholar 

  • Schaller GE, Voesenek LACJ (2015) Focus on ethylene. Plant Physiol 169:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheuring D, Löfke C, Krüger F et al (2016) Actin-dependent vacuolar occupancy of the cell determines auxin-induced growth repression. Proc Natl Acad Sci 113:452–457

    Article  CAS  PubMed  Google Scholar 

  • Schrader J, Baba K, May ST et al (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100:10096–10101. https://doi.org/10.1073/pnas.1633693100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schweingruber F (1996) Tree rings and environment: dendroecology. Paul Haupt, Berne

    Google Scholar 

  • Shaw G (1994) Chemistry of adenine cytokinins. Cytokinins Chem Act Funct. CRC Press, Boca Raton, pp 15–34

    Google Scholar 

  • Sobieszczuk-Nowicka E (2017) Polyamine catabolism adds fuel to leaf senescence. Amino Acids 49:49–56

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Diao Q, Qi H (2015) Polyamine metabolism and biosynthetic genes expression in tomato (Lycopersicon esculentum Mill.) seedlings during cold acclimation. Plant Growth Regul 75:21–32

    Article  CAS  Google Scholar 

  • Sorce C, Giovannelli A, Sebastiani L, Anfodillo T (2013) Hormonal signals involved in the regulation of cambial activity, xylogenesis and vessel patterning in trees. Plant Cell Rep 32:885–898

    Article  CAS  PubMed  Google Scholar 

  • Speer JH (2010) Fundamentals of tree-ring research. University of Arizona Press, Tucson

    Google Scholar 

  • Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500. https://doi.org/10.3732/ajb.93.10.1490

    Article  PubMed  Google Scholar 

  • Spicer R, Holbrook NM (2007) Parenchyma cell respiration and survival in secondary xylem: does metabolic activity decline with cell age? Plant Cell Environ 30:934–943. https://doi.org/10.1111/j.1365-3040.2007.01677.x

    Article  CAS  PubMed  Google Scholar 

  • Stoffel M, Bollschweiler M (2009) What tree rings can tell about earth-surface processes: teaching the principles of dendrogeomorphology. Geogr Compass 3:1013–1037

    Article  Google Scholar 

  • Sundberg B, Uggla C (1998) Origin and dynamics of indoleacetic acid under polar transport in Pinus sylvestris. Physiol Plant 104:22–29. https://doi.org/10.1034/j.1399-3054.1998.1040104.x

    Article  CAS  Google Scholar 

  • Sundberg B, Anthony Little CH, Riding RT, Sandberg G (1987) Levels of endogenous indole-3-acetic acid in the vascular cambium region of Abies balsamea trees during the activity-rest-quiescence transition. Physiol Plant 71:163–170

    Article  CAS  Google Scholar 

  • Sundberg B, Little C, Cui K (1990) Distribution of indole-3-acetic acid and the occurrence of its alkali-labile conjugates in the extraxylary region of Pinus sylvestris stems. Plant Physiol 93:1295–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sundberg B, Little CHA, Cui K, Sandberg G (1991) Level of endogenous indole-3-acetic acid in the stem of Pinus sylvestris in relation to the seasonal variation of cambial activity. Plant Cell Environ 14:241–246. https://doi.org/10.1111/j.1365-3040.1991.tb01342.x

    Article  CAS  Google Scholar 

  • Sundberg B, Ericsson A, Little C et al (1993) The relationship between crown size and ring width in Pinus sylvestris L. stems: dependence on indole-3-acetic acid, carbohydrates and nitrogen in the cambial. Tree Physiol 12:347–362

    Article  CAS  PubMed  Google Scholar 

  • Sundberg B, Uggla C, Tuominen H (2000) Cell and molecular biology of wood formation. In: Savidge R, Barnett J, Napier R (eds) BIOS Scientific Publishers, Oxford, pp 169–188

  • Sundell D, Mannapperuma C, Netotea S et al (2015) The Plant genome integrative explorer resource: PlantGen IE.org. New Phytol 208:1149–1156

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N (2016) Hormone signaling pathways under stress combinations. Plant Signal Behav 11:e1247139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki N, Bassil E, Hamilton JS et al (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS One 11:e0147625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tessier L, Nola P, Serre-Bachet F (1994) Deciduous Quercus in the Mediterranean region: tree-ring/climate relationships. New Phytol 126:355–367

    Article  Google Scholar 

  • Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240:1–18

    Article  CAS  PubMed  Google Scholar 

  • Tong W, Yoshimoto K, Kakehi J-I et al (2014) Thermospermine modulates expression of auxin-related genes in Arabidopsis. Front Plant Sci 5:94

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsuyama T, Kawai R, Shitan N et al (2013) Proton-dependent coniferin transport, a common major transport event in differentiating xylem tissue of woody plants. Plant Physiol 162:918–926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuominen H, Puech L, Fink S, Sundberg B (1997) A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol 115:577–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uggla C, Moritz T, Sandberg G, Sundberg B (1996) Auxin as a positional signal in pattern formation in plants. Proc Natl Acad Sci 93:9282–9286. https://doi.org/10.1073/pnas.93.17.9282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uggla C, Mellerowicz EJ, Sundberg B (1998) Indole-3-acetic acid controls cambial growth in scots pine by positional signaling. Plant Physiol 117:113–121. https://doi.org/10.1104/pp.117.1.113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uggla C, Magel E, Moritz T, Sundberg B (2001) Function and dynamics of auxin and carbohydrates during earlywood/latewood transition in Scots pine. Plant Physiol 125:2029–2039. https://doi.org/10.1104/pp.125.4.2029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unterholzner SJ, Rozhon W, Papacek M et al (2015) Brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell 27:2261–2272. https://doi.org/10.1105/tpc.15.00433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unterholzner SJ, Rozhon W, Poppenberger B (2016) Reply: interaction between brassinosteroids and gibberellins: synthesis or signaling? In arabidopsis, both! Plant Cell 28:836–839. https://doi.org/10.1105/tpc.16.00120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ursache R, Nieminen K, Helariutta Y (2013) Genetic and hormonal regulation of cambial development. Physiol Plant 147:36–45

    Article  CAS  PubMed  Google Scholar 

  • Vaganov EA, Hughes MK, Shashkin AV, Hughes MK (2008) Growth dynamics of conifer tree rings: images of past and future environments. Ecological Studies. Springer, Berlin

    Google Scholar 

  • van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:4749–4761. https://doi.org/10.1093/jxb/err196

    Article  CAS  PubMed  Google Scholar 

  • Van Hautegem T, Waters AJ, Goodrich J, Nowack MK (2015) Only in dying, life: programmed cell death during plant development. Trends Plant Sci 20:102–113

    Article  CAS  PubMed  Google Scholar 

  • Vandepoele K, Saeys Y, Simillion C et al (2002) The automatic detection of homologous regions (ADHoRe) and its application to microcolinearity between Arabidopsis and rice. Genome Res 12:1792–1801. https://doi.org/10.1101/gr.400202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plant 127:167–181

    Article  CAS  Google Scholar 

  • Welling A, Kaikuranta P, Rinne P (1997) Photoperiodic induction of dormancy and freezing tolerance in Betula pubescens. Involvement of ABA and dehydrins. Physiol Plant 100:119–125

    Article  CAS  Google Scholar 

  • Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci 98:10487–10492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wimmer R (2002) Wood anatomical features in tree-rings as indicators of environmental change. Dendrochronologia 20:21–36. https://doi.org/10.1078/1125-7865-00005

    Article  Google Scholar 

  • Wolbang CM, Ross JJ (2001) Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. Planta 214:153–157

    Article  CAS  PubMed  Google Scholar 

  • Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117

    Article  CAS  PubMed  Google Scholar 

  • Xie L, Yang C, Wang X (2011) Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. J Exp Bot 62:4495–4506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong L, Zhu J-K (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto R, Fujioka S, Demura T et al (2001) Brassinosteroid levels increase drastically prior to morphogenesis of tracheary elements. Plant Physiol 125:556–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto R, Fujioka S, Iwamoto K et al (2006) Co-regulation of brassinosteroid biosynthesis-related genes during xylem cell differentiation. Plant Cell Physiol 48:74–83. https://doi.org/10.1093/pcp/pcl039

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi Y, Ogawa M, Kuwahara A et al (2004) Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16:367–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Jia Z, Chen F et al (2015) Natural cold acclimatisation and de-acclimatisation of Magnolia wufengensis in response to alternative methods of application of abscisic acid. J Hortic Sci Biotechnol 90:704–710

    Article  CAS  Google Scholar 

  • Ye Z-H, Zhong R (2015) Molecular control of wood formation in trees. J Exp Bot 66:4119–4131

    Article  CAS  PubMed  Google Scholar 

  • York N, Garden B (2018) Macadamia nut production in the Hawaiian Islands Author (s): R. A. Hamilton and W. B. Storey Published by: Springer on behalf of New York Botanical Garden Press Stable. http://www.jstor.org/stable/4287882. Macadamia Nut Production in the Hawaii, vol 10, pp 92–100

  • Yoshimoto K, Takamura H, Kadota I et al (2016) Chemical control of xylem differentiation by thermospermine, xylemin, and auxin. Sci Rep 6:21487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youn JH, Kim T-W, Joo S-H et al (2018) Function and molecular regulation of DWARF1 as a C-24 reductase in brassinosteroid biosynthesis in Arabidopsis. J Exp Bot 69:1873–1886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarra I, Revilla G, Sampedro J, Valdivia ER (2019) Biosynthesis and regulation of secondary cell wall. Progress in Botany. Springer, Berlin, Heidelberg, pp 1–38

    Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119

    Article  Google Scholar 

  • Zhang J, Elo A, Helariutta Y (2011) Arabidopsis as a model for wood formation. Curr Opin Biotechnol 22:293–299

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Xu P, Wang W et al (2018) Arabidopsis G-protein β subunit AGB1 interacts with BES1 to regulate brassinosteroid signaling and cell elongation. Front Plant Sci 8:2225

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64. https://doi.org/10.1146/annurev-arplant-042809-112308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng J, Xi M, Lü Y et al (2013) Transcriptional analysis provides new insights into cold-and dehydration-tolerance signaling pathways and on regulation of stem cell activity in the vascular cambium of poplar. Plant Mol Biol Report 31:75–86

    Article  CAS  Google Scholar 

  • Zhong R, Cui D, Ye Z-H (2019) Secondary cell wall biosynthesis. New Phytol 221:1703–1723

    Article  CAS  PubMed  Google Scholar 

  • Zhu M, Assmann SM (2017) Metabolic signatures in response to abscisic acid (ABA) treatment in Brassica napus guard cells revealed by metabolomics. Sci Rep 7:12875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwack PJ, Rashotte AM (2013) Cytokinin inhibition of leaf senescence. Plant Signal Behav 8:e24737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was funded by the NSERC Industrial Research Chair. The authors thank Maxence Martin for his precious comments on the first draft of the manuscript, Murray Hay for verifying the English of the text, and the reviewers for their comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Valentina Buttò.

Additional information

Communicated by Marcos Buckeridge.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buttò, V., Deslauriers, A., Rossi, S. et al. The role of plant hormones in tree-ring formation. Trees 34, 315–335 (2020). https://doi.org/10.1007/s00468-019-01940-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-019-01940-4

Keywords