Anatomical, Developmental and Physiological Bases of Tree-Ring Formation in Relation to Environmental Factors
- Rathgeber, Cyrille B. K. 3
- Pérez-de-Lis, Gonzalo 3
- Fernández-de-Uña, Laura 3
- Fonti, Patrick 1
- Rossi, Sergio 56
- Treydte, Kerstin 1
- Gessler, Arthur 12
- Deslauriers, Annie 5
- Fonti, Marina V. 4
- Ponton, Stéphane 3
- 1 Research Unit Forest Dynamics, Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland
- 2 Institute of Terrestrial Ecosystems, ETH Zurich, Zurich, Switzerland
- 3 Université de Lorraine, AgroParisTech, INRAE, SILVA, 54000, Nancy, France
- 4 Laboratory of Ecosystems Biogeochemistry, Institute of Ecology and Geography, Siberian Federal University, Svobodny 79, 660041, Krasnoyarsk, Russia
- 5 Département Des Sciences Fondamentales, Université du Québec À Chicoutimi, Chicoutimi, G72B1, Canada
- 6 Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China
ISSN: 1568-2544
ISBN: 9783030926977, 9783030926984
Ano de publicación: 2022
Páxinas: 61-99
Tipo: Capítulo de libro
Resumo
Understanding the process of wood formation and its dynamics over the growing season is fundamental to interpret the isotopic signature of tree rings. Indeed, the isotopic signal recorded in wood does not only depend on the conditions influencing carbon, water, and nitrogen uptake in the leaves and roots, but also on how these elements are translocated to the stem and incorporated into the developing xylem. Depending on environmental conditions, tree developmental stage, and physiological status, wood formation dynamics can vary greatly and produce tree-ring structures carrying specific isotopic signatures. In this chapter, we present the physiological processes involved in wood formation, along with their relationships with anatomical, developmental, and environmental factors, to understand when and how photosynthetic assimilates are progressively incorporated into the forming xylem, creating the final isotopic signature of a tree ring. First, we review current knowledge on the structure and functions of wood. Then we describe the xylogenesis process (how and when the new xylem cells produced by the cambium develop through successive differentiation phases), and its relationships with physiological, developmental, and environmental factors. Finally, we explain the kinetics of xylem cell differentiation and show why the knowledge recently acquired in this field allows us to better understand the isotopic signals in tree rings.
Referencias bibliográficas
- Anderson DM, Mauk EM, Wahl ER, Morrill C, Wagner AJ, Easterling D, Rutishauser T (2013) Global warming in an independent record of the past 130 years. Geophys Res Lett 40(1):189–193
- Andrianantenaina AN, Rathgeber CBK, Pérez-de-Lis G, Cuny H, Ruelle J (2019) Quantifying intra-annual dynamics of carbon sequestration in the forming wood: a novel histologic approach. Ann for Sci 76:1–12
- Arora R, Rowland LJ, Tanino K (2003) Induction and release of bud dormancy in woody perennials: a science comes of age. HortScience 38:911–921
- Balducci L, Cuny HE, Rathgeber CBK, Deslauriers A, Giovannelli A, Rossi S (2016) Compensatory mechanisms mitigate the effect of warming and drought on wood formation. Plant, Cell Environ 39:1338–1352
- Balzano A, Čufar K, Battipaglia G, Merela M, Prislan P, Aronne G, De Micco V (2018) Xylogenesis reveals the genesis and ecological signal of IADFs in Pinus pinea L. And Arbutus unedo L. And. Annals of Botany 121:1231–1242
- Bamber RK (1976) Heartwood, its function and formation. Wood Sci Technol 10:1–8
- Bamber RK, Fukazawa K (1985) Sapwood and heartwood: a review. Forestry Abstracts 46:567–580
- Barbaroux C, Bréda N (2002) Contrasting distribution and seasonal dynamics of carbohydrate reserves in stem wood of adult ring-porous sessile oak and diffuse-porous beech trees. Tree Physiol 22:1201–1210
- Barbaroux C, Bréda N, Dufrêne E (2003) Distribution of above-ground and below-ground carbohydrate reserves in adult trees of two contrasting broad-leaved species (Quercus petraea and Fagus sylvatica). New Phytol 157:605–615
- Barbour MM, Walcroft AS, Farquhar GD (2002) Seasonal variation in δ13C and δ18O of cellulose from growth rings of Pinus radiata. Plant, Cell Environ 25:1483–1499
- Barnett JR (1981) Secondary xylem cell development. In: Barnett JR (ed) Xylem cell development. Castle House Publications LTD, Tunbridge wells, pp 47–95
- Basler D, Körner C (2014) Photoperiod and temperature responses of bud swelling and bud burst in four temperate forest tree species. Tree Physiol 34:377–388
- Bazot S, Barthes L, Blanot D, Fresneau C (2013) Distribution of non-structural nitrogen and carbohydrate compounds in mature oak trees in a temperate forest at four key phenological stages. Trees-Struct Funct 27:1023–1034
- Begum S, Nakaba S, Oribe Y, Kubo T, Funada R (2010) Changes in the localization and levels of starch and lipids in cambium and phloem during cambial reactivation by artificial heating of main stems of Cryptomeria japonica trees. Ann Bot 106:885–895
- Begum S, Nakaba S, Yamagishi Y, Oribe Y, Funada R (2013) Regulation of cambial activity in relation to environmental conditions: understanding the role of temperature in wood formation of trees. Physiol Plant 147:46–54
- Begum S, Nakaba S, Yamagishi Y, Yamane K, Islam MA, Oribe Y, Ko JH, Jin HO, Funada R (2012) A rapid decrease in temperature induces latewood formation in artificially reactivated cambium of conifer stems. Ann Bot 110:875–885
- Begum S, Shibagaki M, Furusawa O, Nakaba S, Yamagishi Y, Yoshimoto J, Jin HO, Sano Y, Funada R (2012) Cold stability of microtubules in wood-forming tissues of conifers during seasons of active and dormant cambium. Planta 235:165–179
- Belmecheri S, Wright WE, Szejner P, Morino KA, Monson RK (2018) Carbon and oxygen isotope fractionations in tree rings reveal interactions between cambial phenology and seasonal climate. Plant, Cell Environ 41:2758–2772
- Bollhöner B, Prestele J, Tuominen H (2012) Xylem cell death: emerging understanding of regulation and function. J Exp Bot 63:1081–1094
- Bosio F, Rossi S, Marcati CR (2016) Periodicity and environmental drivers of apical and lateral growth in a Cerrado woody species. Trees-Struct Funct 30:1495–1505
- Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178(1):24–40
- Brandes E, Kodama N, Whittaker K, Weston C, Rennenberg H, Keitel C, Adams MA, Gessler A (2006) Short-term variation in the isotopic composition of organic matter allocated from the leaves to the stem of Pinus sylvestris: effects of photosynthetic and postphotosynthetic carbon isotope fractionation. Glob Change Biol 12:1922–1939
- Brett CT (2000) Cellulose microfibrils in plants: Biosynthesis, deposition, and integration into the cell wall. Int Rev Cytol 199:161–199
- Briffa KR, Osborn TJ, Schweingruber FH, Jones PD, Shiyatov SG, Vaganov EA (2002) Tree-ring width and density data around the Northern Hemisphere: Part 1, local and regional climate signals. Holocene 12:737–757
- Briffa KR, Osborn TJ, Schweingruber FH, Jones PD, Shiyatov SG, Vaganov EA (2002) Tree-ring width and density data around the Northern Hemisphere: part 2, spatio-temporal variability and associated climate patterns. Holocene 12:759–789
- Brodribb TJ, Pittermann J, Coomes DA (2012) Elegance versus speed: examining the competition between conifer and angiosperm trees. Int J Plant Sci 173:673–694
- Buttò V, Deslauriers A, Rossi S, Rozenberg P, Shishov V, Morin H (2019a) The role of plant hormones in tree-ring formation. Trees-Struct Funct
- Buttò V, Rossi S, Deslauriers A, Morin H (2019) Is size an issue of time? Relationship between the duration of xylem development and cell traits. Ann Bot 123:1257–1265
- Camarero JJ, Olano JM, Parras A (2010) Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol 185:471–480
- Carvalho A, Nabais C, Vieira J, Rossi S, Campelo F (2015) Plastic response of tracheids in Pinus pinaster in a water-limited environment: adjusting lumen size instead of wall thickness. PLoS ONE 10:1–14
- Cavender-Bares J, Cortes P, Rambal S, Joffre R, Miles B, Rocheteau A (2005) Summer and winter sensitivity of leaves and xylem to minimum freezing temperatures: a comparison of co-occurring Mediterranean oaks that differ in leaf lifespan. New Phytol 168:597–612
- Chaffey NJ (ed) (2002) Wood formation in trees—cell and molecular biology techniques. Taylor and Francis, London, New York, pp 364
- Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366
- Chuine I (2010) Why does phenology drive species distribution? Philos Trans R Soc B: Biol Sci 365:3149–3160
- Cochard H, Froux F, Mayr S, Coutand C (2004) Xylem wall collapse in water-stressed pine needles. Plant Physiol 134:401–408
- Cochard H, Tyree MT (1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiol 6:393–407
- Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol Biochem 38:109–124
- Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326
- Cosgrove DJ, Jarvis MC (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3(204):201–206
- Čufar K, Cherubini M, Gričar J, Prislan P, Spina S, Romagnoli M (2011) Xylem and phloem formation in chestnut (Castanea sativa Mill.) during the 2008 growing season. Dendrochronologia 29:127–134
- Cuny HE, Fonti P, Rathgeber CBK, von Arx G, Peters RL, Frank DC (2019) Couplings in cell differentiation kinetics mitigate air temperature influence on conifer wood anatomy. Plant, Cell Environ 42:1222–1232
- Cuny HE, Rathgeber CBK (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
- Cuny HE, Rathgeber CBK, Frank D, Fonti P, Fournier M (2014) Kinetics of tracheid development explain conifer tree-ring structure. New Phytol 203:1231–1241
- Cuny HE, Rathgeber CBK, Frank D, Fonti P, Makinen H, Prislan P, Rossi S, Del Castillo EMEM, Campelo F, Vavrčík H et al (2015) Woody biomass production lags stem-girth increase by over one month in coniferous forests. Nature Plants 1:1–6
- Cuny HE, Rathgeber CBK, Lebourgeois F, Fortin M, Fournier M (2012) Life strategies in intra-annual dynamics of wood formation: example of three conifer species in a temperate forest in north-east France. Tree Physiol 32:612–625
- De Micco V, Balzano A, Wheeler EA, Baas P (2016) Tyloses and gums: a review of structure, function and occurence of vessel occlusions. IAWA J 37:186–205
- De Micco V, Campelo F, De Luis M, Bräuning A, Grabner M, Battipaglia G, Cherubini P (2016) Intra-annual density fluctuations in tree rings: how, when, where, and why? IAWA J 37:232–259
- De Micco V, Carrer M, Rathgeber CBK, Julio Camarero J, Voltas J, Cherubini P, Battipaglia G (2019) From xylogenesis to tree rings: wood traits to investigate tree response to environmental changes. IAWA J 40:155–182
- Delpierre N, Lireux S, Hartig F, Camarero JJ, Cheaib A, Čufar K, Cuny H, Deslauriers A, Fonti P, Gričar J et al (2019) Chilling and forcing temperatures interact to predict the onset of wood formation in Northern Hemisphere conifers. Glob Change Biol 25:1089–1105
- Delpierre N, Vitasse Y, Chuine I, Guillemot J, Bazot S, Rutishauser T, Rathgeber CBK (2016) Temperate and boreal forest tree phenology: from organ-scale processes to terrestrial ecosystem models. Ann for Sci 73:5–25
- Denne MP, Dodd RS (1981) The environmental control of xylem differentiation. In: Barnett JR (ed) Xylem cell development. Castle House Publications, Tunbridge Wells, pp 236–255
- Deslauriers A, Huang JG, Balducci L, Beaulieu M, Rossi S (2016) The contribution of carbon and water in modulating wood formation in black spruce saplings. Plant Physiol 170:2072–2084
- Dickson A, Nanayakkara B, Sellier D, Meason D, Donaldson L, Brownlie R (2017) Fluorescence imaging of cambial zones to study wood formation in Pinus radiata D. Don. Trees-Struct Funct 31:479–490
- Domec JC, Gartner BL (2002) How do water transport and water storage differ in coniferous earlywood and latewood? J Exp Bot 53(379):2369–2379
- Donaldson LA (1985) Within- and between-tree variation in lignin concentration in the tracheid cell wall of Pinus radiata. NZ J Forest Sci 15:361–369
- Donaldson LA (1987) S3 lignin concentration in radiata pine tracheids. Wood Sci Technol 21:227–234
- Donaldson LA (2001) Lignification and lignin topochemistry—an ultrastructural view. Phytochem 859–873
- Donaldson LA, Baas P (2019) Wood cell wall ultrastructure the key to understanding wood properties and behaviour. IAWA J 40(4):645–672
- El Zein R, Maillard P, Bréda N, Marchand J, Montpied P, Gérant D (2011) Seasonal changes of C and N non-structural compounds in the stem sapwood of adult sessile oak and beech trees. Tree Physiol 31:843–854
- Evert RF (2006) Esau's plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development. John Wiley and Sons, pp 601
- Fagerstedt K, Karkonen A (2015) The plant cell wall. J Integr Plant Biol 57(4):328–329
- Fernández-de-Uña L, Aranda I, Rossi S, Fonti P, Canellas I, Gea-Izquierdo G (2018) Divergent phenological and leaf gas exchange strategies of two competing tree species drive contrasting responses to drought at their altitudinal boundary. Tree Physiol 38(8):1152–1165
- Fernández-de-Uña L, Rossi S, Aranda I, Fonti P, González-González BD, Cañellas I, Gea-Izquierdo G (2017) Xylem and leaf functional adjustments to drought in Pinus sylvestris and Quercus pyrenaica at their elevational boundary. Front Plant Sci 8(1200):1201–1212
- Fonti MV, Vaganov EA, Wirth C, Shashkin AV, Astrakhantseva NV, Schulze E-D (2018) Age-effect on intra-annual δ13C-variability within Scots Pine tree-rings from Central Siberia. For 9(364):1–14
- Fonti P, Von Arx G, García-González I, Eilmann B, Sass-Klaassen U, Gärtner H, Eckstein D (2010) Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytol 185:42–53
- Fournier M, Moulia B, Stokes A, Coutand C, Fourcaud T (2006) Tree biomechanics and growth strategies in the context of forest functional ecology. In: Speck T, Rowe NP (eds) Herrel A. CRC Press, Ecology and biomechanics. a mechanical approach to the ecology of animals and plants. Boca Raton, pp 1–33
- Freudenberg K (1959) Biosynthesis and constitution of lignin. Nature 183:1152–1155
- Fritts HC (1976) Tree rings and climate. Academic Press, London, pp 582
- Fromm J (2013) Xylem development in trees: from cambial division to mature wood cells. In: Fromm J (ed) Cellular aspect of wood formation. Springer-Verlag, Berlin, Heidelberg, New York, Dordrecht, London, pp 3–39
- Gessler A, Ferrio JP, Hommel R, Treydte K, Werner RA, Monson RK (2014) Stable isotopes in tree rings: towards a mechanistic understanding of isotope fractionation and mixing processes from the leaves to the wood. Tree Physiol 34:796–818
- Gindl W, Grabner M, Wimmer R (2000) The influence of temperature on latewood lignin content in treeline Norway spruce compared with maximum density and ring width. Trees-Struct Funct 14:409–414
- Gričar J, Čufar K (2008) Seasonal dynamics of phloem and xylem formation in silver fir and Norway spruce as affected by drought. Russ J Plant Physiol 55:538–543
- Gričar J, Krže L, Čufar K (2009) Number of cells in xylem, phloem and dormant cambium in silver fir (Abies alba), in trees of different vitality. IAWA J 30:121–133
- Gričar J, Lavrič M, Ferlan M, Vodnik D, Eler K (2017) Intra-annual leaf phenology, radial growth and structure of xylem and phloem in different tree parts of Quercus pubescens. Eur J Forest Res 136:625–637
- Gričar J, Zupančič M, Čufar K, Oven P (2007) Regular cambial activity and xylem and phloem formation in locally heated and cooled stem portions of Norway spruce. Wood Sci Technol 41:463–475
- Gričar J, Zupančič M, Čufar K, Oven P (2007) Wood formation in Norway Spruce (Picea abies) studied by pinning and intact tissue sampling method. Wood Res 52:1–10
- Grillos SJ, Smith FH (1959) The secondary phloem of Douglas-fir. For Sci 5(4):377–388
- Groover A, Jones AM (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 119:375–384
- Gruber A, Strobl S, Veit B, Oberhuber W (2010) Impact of drought on the temporal dynamics of wood formation in Pinus sylvestris. Tree Physiol 30:490–501
- Gyllenstrand N, Clapham D, Källman T, Lagercrantz U (2007) A Norway spruce FLOWERING LOCUS T homolog is implicated in control of growth rhythm in conifers. Plant Physiol 144:248–257
- Helle G, Schleser GH (2004) Beyond CO2-fixation by Rubisco—an interpretation of 13C/12C variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant, Cell Environ 27:367–380
- Hillis WE (1987) Heartwood and tree exudates. Springer-Verlag, Berlin, Heidelberg, pp 268
- Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant, Cell Environ 26:1067–1081
- Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540
- Hsiao TC (1973) Plant responses to water stress. Annu Rev Plant Physiol 24:519–570
- Jansen S, Baas P, Gasson P, Lens F, Smets E (2004) Variation in xylem structure from tropics to tundra: evidence from vestured pits. Proc Natl Acad Sci USA 101:8833–8837
- Johnson DM, Büntgen U, Frank DC, Kausrud K, Haynes KJ, Liebhold AM, Esper J, Stenseth NC (2010) Climatic warming disrupts recurrent Alpine insect outbreaks. Proc Natl Acad Sci USA 107:20576–20581
- Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125:94–97
- Kagawa A, Sugimoto A, Maximov TC (2006) 13CO2 pulse-labelling of photoassimilates reveals carbon allocation within and between tree rings. Plant, Cell Environ 29:1571–1584
- Keegstra K (2010) Plant cell walls. Plant Physiol 154:483–486
- Koch G, Schmitt U (2013) Topochemical and electron microscopic analyses on the lignification of individual cell wall layers during wood formation and secondary changes. In: Fromm J (ed) Cellular aspect of wood formation. Springer-Verlag, Berlin, Heidelberg, New York, Dordrecht, London, pp 41–69
- Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246
- Konôpka B, Yuste JC, Janssens IA, Ceulemans R (2005) Comparison of fine root dynamics in Scots pine and Pedunculate oak in sandy soil. Plant Soil 276:33–45
- Kozlowski TT, Pallardy SG (1996) The physiological ecology of woody plants. Academic Press, San Diego, London, Boston, New York, Sydney, Tokyo, Toronto, pp 411
- Kozlowski TT, Winget CH (1964) Diurnal and seasonal variation in radii of tree stems. Ecol 45(1):149–155
- Kramer PJ (1964) The role of water in wood formation. In: Zimmermann MH (ed) The formation of wood in forest trees. Academic Press, New York, London, pp 519–532
- Kuroda K, Yamashita K, Fujiwara T (2009) Cellular level observation of water loss and the refilling of tracheids in the xylem of Cryptomeria japonica during heartwood formation. Trees-Struct Funct 23:1163–1172
- Lachaud S, Catesson AM, Bonnemain JL (1999) Structure and functions of the vascular cambium. Comptes Rendus de l'Academie des Sciences—Serie III, vol 322, pp 633–650
- Lachenbruch B, Moore JR, Evans R (2011) Radial variation in wood structure and function in woody plants, and hypotheses for its occurrence. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size- and age-related changes in tree structure and function. Springer, Dordrecht, pp 121–164
- Ladefoged K (1952) The periodicity of wood formation. Kobenhavn: Det Kongelige danske videnskabernes selskab, pp 98
- Larson PR (1994) The vascular cambium. Development and structure. Springer-Verlag, Berlin, Heidelberg, New York, London, Paris, Tokyo, Hong Kong, Barcelona, Budapest, pp 725
- Lavrič M, Eler K, Ferlan M, Vodnik D, Gričar J (2017) Chronological sequence of leaf phenology, xylem and phloem formation and sap flow of Quercus pubescens from abandoned karst grasslands. Front Plant Sci 8:1–11
- Lemay A, Krause C, Rossi S, Achim A (2017) Xylogenesis in stems and roots after thinning in the boreal forest of Quebec. Canada. Tree Physiol 37(11):1554–1563
- Little CHA, Bonga JM (1974) Rest in cambium of Abies balsamea. Can J Bot 52(7):1723–1730
- Lundmark T, Bergh J, Strand M, Koppel A (1998) Seasonal variation of maximum photochemical efficiency in boreal Norway spruce stands. Trees-Struct Funct 13:63–67
- Lupi C, Morin H, Deslauriers A, Rossi S (2010) Xylem phenology and wood production: resolving the chicken-or-egg dilemma. Plant, Cell Environ 33:1721–1730
- Lyr H, Hoffmann G (1967) Growth rates and growth periodicity of tree roots. Int Rev For Res 181–236
- McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quatern Sci Rev 23:771–801
- McCormack LM, Adams TS, Smithwick EAH, Eissenstat DM (2014) Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecol 95:2224–2235
- Mellerowicz EJ, Sundberg B (2008) Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Curr Opin Plant Biol 11:293–300
- Michelot A, Simard S, Rathgeber C, Dufrêne E, Damesin C (2012) Comparing the intra-annual wood formation of three European species (Fagus sylvatica, Quercus petraea and Pinus sylvestris) as related to leaf phenology and non-structural carbohydrate dynamics. Tree Physiol 32:1033–1045
- Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095
- Millard P, Proe MF (1992) Storage and internal cycling of nitrogen in relation to seasonal growth of Sitka spruce. Tree Physiol 10:45–48
- Moser L, Fonti P, Büntgen U, Esper J, Luterbacher J, Franzen J, Frank D (2009) Timing and duration of European larch growing season along altitudinal gradients in the Swiss Alps. Tree Physiol 30:225–233
- Mutwil M, Debolt S, Persson S (2008) Cellulose synthesis: a complex complex. Curr Opin Plant Biol 11:252–257
- Nonami H, Boyer JS (2008) Turgor and growth at low water potentials. Plant Physiol 89:798–804
- Notaguchi M, Okamoto S (2015) Dynamics of long-distance signaling via plant vascular tissues. Front Plant Sci 6:161
- O'Neill MA, York WS (2009) The plant cell wall. Annu Plant Rev 1–44
- Ogaya R, Penuelas J (2004) Phenological patterns of Quercus ilex, Phillyrea latifolia, and Arbutus unedo growing under a field experimental drought. Ecoscience 11:263–270
- Ogée J, Barbour MM, Wingate L, Bert D, Bosc A, Stievenard M, Lambrot C, Pierre M, Bariac T, Loustau D et al (2009) A single-substrate model to interpret intra-annual stable isotope signals in tree-ring cellulose. Plant, Cell Environ 32:1071–1090
- Ohashi S, Kuroda K, Takano T, Suzuki Y, Fujiwara T, Abe H, Kagawa A, Sugiyama M, Kubojima Y, Zhang C et al (2017) Temporal trends in 13C concentrations in the bark, sapwood, heartwood, and whole wood of four tree species in Japanese forests from 2011 to 2016. J Environ Radioact 178–179:335–342
- 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
- Oribe Y, Kubo T (1997) Effect of heat on cambial reactivation during winter dormancy in evergreen and deciduous conifers. Tree Physiol 17(2):81–87
- Pérez-de-Lis G, Olano JM, Rozas V, Rossi S, Vázquez-Ruiz RA, García-González I (2017) Environmental conditions and vascular cambium regulate carbon allocation to xylem growth in deciduous oaks. Funct Ecol 31:592–603
- Pérez-de-Lis G, Rossi S, Vázquez-Ruiz RA, Rozas V, García-González I (2016) Do changes in spring phenology affect earlywood vessels? Perspective from the xylogenesis monitoring of two sympatric ring-porous oaks. New Phytol 209:521–530
- Pérez-de-Lis G, Rozas V, Vázquez-Ruiz RA, García-González I (2018) Do ring-porous oaks prioritize earlywood vessel efficiency over safety? Environmental effects on vessel diameter and tyloses formation. Agric for Meteorol 248:205–214
- Perrin M, Rossi S, Isabel N (2017) Synchronisms between bud and cambium phenology in black spruce: Early-flushing provenances exhibit early xylem formation. Tree Physiol 37:593–603
- Pesquet E, Zhang B, Gorzsas A, Puhakainen T, Serk H, Escamez S, Barbier O, Gerber L, Courtois-Moreau C, Alatalo E et al (2013) Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell 25(4):1314–1328
- Piermattei A, Crivellaro A, Carrer M, Urbinati C (2015) The “blue ring”: anatomy and formation hypothesis of a new tree-ring anomaly in conifers. Trees-Struct Funct 29:613–620
- Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 127(4):1513–1523
- Pratt RB, Jacobsen AL, Ewers FW, Davis SD (2007) Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparral. New Phytol 174:787–798
- Prislan P, Čufar K, Koch G, Schmitt U, Gričar J (2013) Review of cellular and subcellular changes in the cambium. IAWA J 34:391–407
- Prislan P, Gričar J, de Luis M, Smith KT, Čufar K (2013) Phenological variation in xylem and phloem formation in Fagus sylvatica from two contrasting sites. Agric for Meteorol 180:142–151
- Prislan P, Mrak P, Žnidaršič N, Štrus J, Humar M, Thaler N, Mrak T, Gričar J (2018) Intra-annual dynamics of phloem formation and ultrastructural changes in sieve tubes in Fagus sylvatica. Tree Physiol 39:262–274
- Rathgeber CBK, Cuny HE, Fonti P (2016) Biological basis of tree-ring formation: a crash course. Front Plant Sci 7:734
- Rathgeber CBK, Decoux V, Leban JM (2006) Linking intra-tree-ring wood density variations and tracheid anatomical characteristics in Douglas fir (Pseudotsuga menziesii (Mirb.) Franco). Ann for Sci 63:699–706
- Rathgeber CBK, Longuetaud F, Mothe F, Cuny H, Le Moguédec G (2011) Phenology of wood formation: Data processing, analysis and visualisation using R (package CAVIAR). Dendrochronologia 29:139–149
- Rathgeber CBK, Rossi S, Bontemps JD (2011) Cambial activity related to tree size in a mature silver-fir plantation. Ann Bot 108:429–438
- Rinne KT, Saurer M, Kirdyanov AV, Loader NJ, Bryukhanova MV, Werner RA, Siegwolf RTW (2015) The relationship between needle sugar carbon isotope ratios and tree rings of larch in Siberia. Tree Physiol 35:1192–1205
- Rohde A, Bastien C, Boerjan W (2011) Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiol 31:472–482
- Rossi S, Anfodillo T, Čufar K, Cuny HE, Deslauriers A, Fonti P, Frank D, Gričar J, Gruber A, Huang JG et al (2016) Pattern of xylem phenology in conifers of cold ecosystems at the Northern Hemisphere. Glob Change Biol 22:3804–3813
- Rossi S, Anfodillo T, Cufar K, Cuny HE, Deslauriers A, Fonti P, Frank D, Gricar J, Gruber A, King GM et al (2013) A meta-analysis of cambiumphenology and growth: linear and non-linear patterns in conifers of the northern hemisphere. Ann Bot 112:1911–1920
- Rossi S, Deslauriers A, Anfodillo T (2006) Assessment of cambial activity and xylogenesis by microsampling tree species: an example at the Alpine timberline. IAWA J 27:383–394
- Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007) Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152:1–12
- Rossi S, Deslauriers A, Anfodillo T, Morin H, Saracino A, Motta R, Borghetti M (2006) Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytol 170:301–310
- Rossi S, Deslauriers A, Griçar J, Seo JW, Rathgeber CBK, Anfodillo T, Morin H, Levanic T, Oven P, Jalkanen R (2008) Critical temperatures for xylogenesis in conifers of cold climates. Glob Ecol Biogeogr 17:696–707
- Rossi S, Morin H, Deslauriers A (2012) Causes and correlations in cambium phenology: towards an integrated framework of xylogenesis. J Exp Bot 63:2117–2126
- Rossi S, Rathgeber CBK, Deslauriers A (2009) Comparing needle and shoot phenology with xylem development on three conifer species in Italy. Ann for Sci 66:206
- Rossi S, Simard S, Rathgeber CBK, Deslauriers A, De Zan C (2009b) Effects of a 20-day-long dry period on cambial and apical meristem growth in Abies balsamea seedlings. Trees-Struct Funct 23:85–93
- Rowe N, Speck T (2005) Plant growth forms: an ecological and evolutionary perspective. New Phytol 166:61–72
- Saderi S, Rathgeber CBK, Rozenberg P, Fournier M (2019) Phenology of wood formation in larch (Larix decidua Mill.) trees growing along a 1000-m elevation gradient in the French Southern Alps. Ann for Sci 76:1–17
- Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289
- Schenker G, Lenz A, Körner C, Hoch G (2014) Physiological minimum temperatures for root growth in seven common European broad-leaved tree species. Tree Physiol 34:302–313
- Schollaen K, Heinrich I, Helle G (2014) UV-laser-based microscopic dissection of tree rings—a novel sampling tool for δ13C and δ18O studies. New Phytol 201:1045–1055
- Schopfer P (2006) Biomechanics of plant growth. Am J Bot 93:1415–1425
- Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G (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
- Schulze B, Wirth C, Linke P, Brand WA, Kuhlmann I, Horna V, Schulze ED (2004) Laser ablation-combustion-GC-IRMS—a new method for online analysis of intra-annual variation of δ13C in tree rings. Tree Physiol 24:1193–1201
- Schweingruber FH (1996) Tree rings and environment. Dendroecology. Berne, Stuttgart, Vienna: Haupt Paul, Swiss federal institute for forest, snow and landscape research, WSL/FNP, Birmensdorf, pp 609
- Schweingruber FH (2007) Wood structure and environment. Springer-Verlag, Berlin, Heidelberg
- Siau JF (1984) Transport processes in wood. Springer, Berlin, Heidelberg, New York, Tokyo, pp 245
- Siddiqui KM (1976) Relationship between cell wall morphology and chemical composition of earlywood and latewood in two coniferous species. Pak J For 26:21–34
- Skene DS (1969) The period of time taken by cambial derivatives to grow and differentiate into Tracheids in Pinus radiata. Ann Bot 33:253–262
- Skene DS (1972) The kinetics of tracheid development in Tsuga canadensis Carr. and its relation to tree vigour. Ann Bot 36:179–187
- Smith RA, Schuetz M, Roach M, Mansfield SD, Ellis B, Samuels L (2013) Neighboring parenchyma cells contribute to Arabidopsis xylem lignification, while lignification of interfascicular fibers is cell autonomous. Plant Cell 25:3988–3999
- Speck T, Burgert I (2011) Plant stems: functional design and mechanics. Annu Rev Mater Res 41:169–193
- Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500
- Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant, Cell Environ 31:632–645
- Sperry JS, Sullivan JEM (1992) Xylem embolism in response to freeze-thaw cycles and water-stress in ring-porous, diffuse-porous, and conifer species. Plant Physiol 100(2):605–613
- Swidrak I, Gruber A, Oberhuber W (2014) Xylem and phloem phenology in co-occurring conifers exposed to drought. Trees-Struct Funct 28:1161–1171
- Taiz L, Zeiger E (2010) Plant Physiology. Sinauer Associates Inc., Sunderland, pp 782
- Takahashi K, Koike S (2014) Altitudinal differences in bud burst and onset and cessation of cambial activity of four subalpine tree species. Landsc Ecol Eng 10:349–354
- Taylor AM, Gartner BL, Morrell JJ (2002) Heartwood formation and natural durability—a review. Wood Fiber Sci 34:587–611
- Thibeault-Martel M, Krause C, Morin H, Rossi S (2008) Cambial activity and intra-annual xylem formation in roots and stems of Abies balsamea and Picea mariana. Ann Bot 102:667–674
- Treydte K, Boda S, Graf Pannatier E, Fonti P, Frank D, Ullrich B, Saurer M, Siegwolf R, Battipaglia G, Werner W et al (2014) Seasonal transfer of oxygen isotopes from precipitation and soil to the tree ring: source water versus needle water enrichment. New Phytol 202:772–783
- Tyree MT, Dixon MA (1986) Water-stress induced cavitation and embolism in some woody-plants. Physiol Plant 66(3):397–405
- Ursache R, Nieminen K, Helariutta Y (2013) Genetic and hormonal regulation of cambial development. Physiol Plant 147:36–45
- Vaganov EA, Hughes MK, Shashkin AV (2006) Growth dynamics of conifer tree rings: images of past and future environments. Springer-Verlag, Berlin, Heidelberg, pp 351
- Vieira J, Rossi S, Campelo F, Freitas H, Nabais C (2014) Xylogenesis of Pinus pinaster under a Mediterranean climate. Ann for Sci 71(1):71–80
- Vincent-Barbaroux C, Berveiller D, Lelarge-Trouverie C, Maia R, Máguas C, Pereira J, Chaves MM, Damesin C (2019) Carbon-use strategies in stem radial growth of two oak species, one Temperate deciduous and one Mediterranean evergreen: what can be inferred from seasonal variations in the δ13C of the current year ring? Tree Physiol 39:1329–1341
- Weigt RB, Bräunlich S, Zimmermann L, Saurer M, Grams TEE, Dietrich HP, Siegwolf RTW, Nikolova PS (2015) Comparison of δ18O and δ13C values between tree-ring whole wood and cellulose in five species growing under two different site conditions. Rapid Commun Mass Spectrom 29:2233–2244
- Wilson AT, Grinsted MJ (1977) 12C/13C in cellulose and lignin as palaeothermometers. Nature 265(5590):133–135
- Wilson JW (1970) The growing tree. The University of Massachusetts Press, Amherst, pp 152
- Wilson JW, Wodzicki T, Zahner R (1966) Differentiation of cambial derivatives: proposed terminology. For Sci 12:438–440
- Wimmer R, Grabner M (2000) A comparison of tree-ring features in Picea abies as correlated with climate. IAWA J 21:403–416
- Wodzicki TJ (1971) Mechanism of xylem differentiation in Pinus silvestris L. J Exp Bot 22:670–687
- Wright SJ, Cornejo FH (1990) Seasonal drought and leaf fall in a tropical forest. Ecol 71:1165–1175
- Yoshimura K, Hayashi S, Takao I, Shimaji K (1981) Studies on the improvement of the pinning method for marking xylem growth I. Minute examination of pin marks in Taeda Pine and other species. Wood Res 67:1–16
- Zalloni E, de Luis M, Campelo F, Novak K, De Micco V, Di Filippo A, Vieira J, Nabais C, Rozas V, Battipaglia G (2016) Climatic signals from intra-annual density fluctuation frequency in Mediterranean pines at a regional scale. Front Plant Sci 7:1–11
- Zeng X, Liu X, Treydte K, Evans MN, Wang W, An W, Sun W, Xu G, Wu G, Zhang X (2017) Climate signals in tree-ring δ18O and δ13C from southeastern Tibet: insights from observations and forward modelling of intra- to interdecadal variability. New Phytol 216:1104–1118
- Zhong R, Ye Z-H (2009) Secondary cell walls. Encycl Life Sci 1–9
- Zimmermann MH (1982) Functional xylem anatomy of angiosperm trees. Baas, P. Springer, New perspectives in wood anatomy. Forestry sciences. Dordrecht, pp 59–70
- Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, Berlin, Heidelberg, New York, Tokyo, pp 146
- Zweifel R (2016) Radial stem variations—a source of tree physiological information not fully exploited yet. Plant Cell & Environ 39(2):231–232
- Zwieniecki MA, Holbrook NM (2000) Bordered pit structure and vessel wall surface properties. Implications for embolism repair. Plant Physiol 123 (3):1015–1020