Winter-spring temperature pattern is closely related to the onset of cambial reactivation in stems of the evergreen conifer Chamaecyparis pisifera.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
31 08 2020
31 08 2020
Historique:
received:
09
12
2019
accepted:
10
06
2020
entrez:
2
9
2020
pubmed:
2
9
2020
medline:
16
3
2021
Statut:
epublish
Résumé
Temperature is an important factor for the cambial growth in temperate trees. We investigated the way daily temperatures patterns (maximum, average and minimum) from late winter to early spring affected the timing of cambial reactivation and xylem differentiation in stems of the conifer Chamaecyparis pisifera. When the daily temperatures started to increase earlier from late winter to early spring, cambial reactivation occurred earlier. Cambium became active when it achieves the desired accumulated temperature above the threshold (cambial reactivation index; CRI) of 13 °C in 11 days in 2013 whereas 18 days in 2014. This difference in duration required for achieving accumulated temperature can be explained with the variations in the daily temperature patterns in 2013 and 2014. Our formula for calculation of CRI predicted the cambial reactivation in 2015. A hypothetical increase of 1-4 °C to the actual daily maximum temperatures of 2013 and 2014 shifted the timing of cambial reactivation and had different effects on cambial reactivation in the two consecutive years because of variations in the actual daily temperatures patterns. Thus, the specific annual pattern of accumulation of temperature from late winter to early spring is a critical factor in determining the timing of cambial reactivation in trees.
Identifiants
pubmed: 32868796
doi: 10.1038/s41598-020-70356-9
pii: 10.1038/s41598-020-70356-9
pmc: PMC7458908
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
14341Références
Funada, R. & Kajita, S. Improvement of woody biomass. In Research Approaches to Sustainable Biomass Systems (ed. Hirasawa, T.) 88–98 (Academic Press, Elsevier, London, 2014).
Funada, R. et al. Xylogenesis in trees: from cambial cell division to cell death. In Secondary Xylem Biology: Origins, Functions and Applications (eds Kim, Y. S. et al.) 25–58 (Academic Press, Elsevier, New York, 2016).
Miyashima, S., Sebastian, J., Lee, J. Y. & Helariutta, Y. Stem cell function during plant vascular development. EMBO J. 32, 178–193 (2013).
pubmed: 23169537
Catesson, A. M. Cambial ultrastructure and biochemistry: changes in relation to vascular tissue differentiation and the seasonal cycle. Int. J. Plant Sci. 155, 251–261 (1994).
Prislan, P., Čufar, K., Koch, G., Schmitt, U. & Gričar, J. Review of cellular and subcellular changes in the cambium. IAWA J. 34, 391–407 (2013).
Begum, S., Nakaba, S., Yamagishi, Y., Oribe, Y. & Funada, R. Regulation of cambial activity in relation to environmental conditions: understanding the role of temperature in wood formation of trees. Physiol. Plant. 147, 46–54 (2013).
pubmed: 22680337
Begum, S. et al. Climate change and the regulation of wood formation in trees by temperature. Trees 32, 3–15 (2018).
Kitin, P. & Funada, R. Earlywood vessels in ring-porous trees become functional for water transport after bud burst and before the maturation of the current-year leaves. IAWA J. 37, 315–331 (2016).
Rossi, S., Morin, H., Deslauriers, A. & Plourde, P. Y. Predicting xylem phenology in black spruce under climate warming. Global Change Biol. 17, 614–625 (2011).
Rossi, S., Girard, M. J. E. E. & Morin, H. Lengthening of the duration of xylogenesis engenders disproportionate increases in xylem production. Global Change Biol. 20, 2261–2271 (2014).
Lupi, C., Morin, H., Deslauriers, A. & Rossi, S. Xylem phenology and wood production: resolving the chicken-or-egg dilemma. Plant Cell Environ. 33, 1721–1730 (2010).
pubmed: 20525004
Begum, S. et al. Temperature responses of cambial reactivation and xylem differentiation in hybrid poplar (Populus sieboldii × P. grandidentata) under natural conditions. Tree Physiol. 28, 1813–1819 (2008).
pubmed: 19193564
Denne, M. P. & Dodd, R. S. The environmental control of xylem differentiation. In Xylem Cell Development (ed. Barnett, J. R.) 236–255 (Castle House Publications, Tunbridge Wells, 1981).
Schweingruber, F. H. Tree rings: Basics and Applications of Dendrochronology (Kluwer Academic Publishers, Dordrecht, 1988).
Huang, J. G., Bergeron, Y., Zhai, L. & Denneler, B. Variation in intra-annual radial growth (xylem formation) of Picea mariana (Pinaceae) along a latitudinal gradient in western Quebec,Canada. Am. J. Bot. 98, 792–800 (2011).
pubmed: 21613181
Shestakova, T. A. et al. Forests synchronize their growth in contrasting Eurasian regions in response to climate warming. Proc. Nat. Acad. Sci. USA 113, 662–667 (2016).
pubmed: 26729860
Li, X. et al. Critical minimum temperature limits xylogenesis and maintains treelines on the southeastern Tibetan Plateau. Sci. Bull. 62, 804–812 (2017).
Liu, S. et al. Differences in xylogenesis between dominant and suppressed trees. Am. J. Bot. 105, 950–956 (2018).
pubmed: 29874391
Ren, P. et al. Critical temperature and precipitation thresholds for the onset of xylogenesis of Juniperus przewalskii in a semi-arid area of the north-eastern Tibetan Plateau. Ann. Bot. 121, 617–624 (2018).
pubmed: 29300821
Zeng, Q., Rossi, S. & Yang, B. Effects of age and size on xylem phenology in two conifers of northwestern China. Front. Plant Sci. 8, 2264 (2018).
pubmed: 29379517
pmcid: 5771374
Giagli, K., Gricar, J., Vavrcik, H. & Gryc, V. Nine-year monitoring of cambial seasonality and cell production in norway spruce. iForest-Biogeosci. For 9, 375–382 (2016).
Castagneri, D., Fonti, P., Arx, G. V. & Carrer, M. How does climate influence xylem morphogenesis over the growing season? Insights from long-term intra-ring anatomy in Picea abies. Ann. Bot. 119, 1011–1020 (2017).
pubmed: 28130220
pmcid: 5604563
Schmitt, U., Jalkanen, R. & Eckstein, D. Cambium dynamics of Pinus sylvestris and Betula spp. in the northern boreal forest in Finland. Silva Fennica 38, 167–178 (2004).
Rathgeber, C. B. K., Rossi, S. & Bontemps, J.-D. Cambial activity related to tree size in a mature silver-fir plantation. Ann. Bot. 108, 429–438 (2011).
pubmed: 21816842
pmcid: 3158687
Treml, V., Kašpar, J., Kuželová, H. & Gryc, V. Differences in intra-annual wood formation in Picea abies across the treeline ecotone, Giant Mountains Czech Republic. Trees 29, 515–526 (2015).
Vieira, J. et al. Adjustment capacity of maritime pine cambial activity in drought-prone environments. PLoS ONE 10, e0126223 (2015).
pubmed: 25961843
pmcid: 4427410
Zhang, J. et al. Cambial phenology in Juniperus przewalskii along different altitudinal gradients in a cold and arid region. Tree Physiol. 38, 840–852 (2018).
pubmed: 29401316
Zhang, J., Gou, X., Manzanedo, R. D., Zhang, F. & Pederson, N. Cambial phenology and xylogenesis of Juniperus przewalskii over a climatic gradient is influenced by both temperature and drought. Agric. For. Meteorol. 260–261, 165–175 (2018).
Funada, R., Kubo, T. & Fushitani, M. Early and latewood formation in Pinus densiflora trees with different amounts of crown. IAWA Bull. New Ser. 11, 281–288 (1990).
Rossi, S. et al. A meta-analysis of cambium phenology and growth: linear and non-linear patterns in conifers of the northern hemisphere. Ann. Bot. 112, 1911–1920 (2013).
pubmed: 24201138
pmcid: 3838565
Savidge, R. A. & Wareing, P. F. Plant growth regulators and the differentiation of vascular elements. In Xylem Cell Development (ed. Barnett, J. R.) 192–235 (Tunbridge Wells, Castle House, 1981).
Barnett, J. R. & Miller, H. The effect of applied heat on graft union formation in dormant Picea sitchensis (Bong.) Carr. J. Exp. Bot. 45, 135–143 (1994).
Oribe, Y. & Kubo, T. Effect of heat on cambial reactivation during winter dormancy in evergreen and deciduous conifers. Tree Physiol. 17, 81–87 (1997).
pubmed: 14759877
Oribe, Y., Funada, R., Shibagaki, M. & Kubo, T. Cambial reactivation in locally heated stems of the evergreen conifer Abies sachalinensis (Schmidt) Masters. Planta 212, 684–691 (2001).
pubmed: 11346941
Oribe, Y., Funada, R. & Kubo, T. 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 (2003).
Gričar, J. et al. Effect of local heating and cooling on cambial activity and cell differentiation in the stem of Norway spruce (Picea abies). Ann. Bot. 97, 943–951 (2006).
pubmed: 16613904
pmcid: 2803384
Begum, S., Nakaba, S., Oribe, Y., Kubo, T. & Funada, R. Cambial sensitivity to rising temperatures by natural condition and artificial heating from late winter to early spring in the evergreen conifer Cryptomeria japonica. Trees 24, 43–52 (2010).
Rahman, M. H. et al. 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 (2016).
Rahman, M. H. et al. Effects of auxin-transport-inhibitor and defoliation on wood formation in locally-heated Abies homolepis. IAWA J. 39, 353–371 (2018).
Oribe, Y. & Funada, R. Locally heated dormant cambium can re-initiate cell production independently of new shoot growth in deciduous conifers (Larix kaempferi). Dendrochronologia 46, 14–23 (2017).
Begum, S., Nakaba, S., Oribe, Y., Kubo, T. & Funada, R. Induction of cambial reactivation by localized heating in a deciduous hardwood hybrid poplar (Populus sieboldii × P. grandidentata). Ann. Bot. 100, 439–447 (2007).
pubmed: 17621596
pmcid: 2533603
Kudo, K. et al. The effects of localized heating and disbudding on cambial reactivation and formation of earlywood vessels in seedlings of the deciduous ring- porous hardwood, Quercus serrata. Ann. Bot. 113, 1021–1027 (2014).
pubmed: 24685716
pmcid: 3997643
IPCC [International Panel on Climate Change]. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (ed Stocker T. F. et al.) (Cambridge University Press, New York, 2013).
Rossi, S. et al. Pattern of xylem phenology in conifers of cold ecosystems at the northern hemisphere. Global Change Biol. 22, 3804–3813 (2016).
Yang, B. et al. New perspective on spring vegetation phenology and global climate change based on Tibetan Plateau tree-ring data. Proc. Nat. Acad. Sci. USA 114, 6966–6971 (2017).
pubmed: 28630302
Delpierre, N. et al. Chilling and forcing temperatures interact to predict the onset of wood formation in Northern Hemisphere conifers. Global Change Biol. 25, 1089–1105 (2019).
Antonucci, S., Rossi, S., Lombardi, F., Marchetti, M. & Tognetti, R. Influence of climatic factors on silver fir xylogenesis along the Italian Peninsula. IAWA J. 40, 259–275 (2019).
De Micco, V. et al. From xylogenesis to tree rings: wood traits to investigate tree response to environmental changes. IAWA J. 40, 155–182 (2019).
Wang, J. Y. A critique of the heat unit approach to plant response studies. Ecology 41, 785–790 (1960).
Moser, L. et al. Timing and duration of European larch growing season along altitudinal gradients in the Swiss Alps. Tree Physiol. 30, 225–233 (2010).
pubmed: 20008326
Romagnolia, M., Moronia, S., Recanatesib, F., Salvatia, R. & Mugnozzaa, G. S. Climate factors and oak decline based on tree-ring analysis. A case study of peri-urban forest in the Mediterranean area. Urban For. Urban Green. 34, 17–28 (2018).
Gruber, A., Pirkebner, D. & Oberhuber, W. Seasonal dynamics of mobile carbohydrate pools in phloem and xylem of two alpine timberline conifers. Tree Physiol. 33, 1076–1083 (2013).
pubmed: 24186941
pmcid: 4816195
Antonucci, S. et al. Synchronisms and correlations of spring phenology between apical and lateral meristems in two boreal conifers. Tree Physiol. 35, 1086–1094 (2015).
pubmed: 26377874
Rossi, S. et al. Critical temperatures for xylogenesis in conifers of cold climates. Global Ecol. Biogeogr. 17, 696–707 (2008).
Li, X. et al. Age dependence of xylogenesis and its climatic sensitivity in smith fir on the south-eastern Tibetan Plateau. Tree Physiol. 33, 48–56 (2013).
pubmed: 23185065
Mencuccini, M. et al. Size-mediated ageing reduces vigour in trees. Ecol. Lett. 8, 1183–1190 (2005).
pubmed: 21352442
Begum, S., Nakaba, S., Oribe, Y., Kubo, T. & Funada, R. 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 (2010).
pubmed: 21037242
pmcid: 2990657
Deslauriers, A., Rossi, S., Anfodillo, T. & Saracino, A. Cambial phenology, wood formation and temperature thresholds in two contrasting years at high altitude in southern Italy. Tree Physiol. 28, 863–871 (2008).
pubmed: 18381267
Rossi, S., Deslauriers, A., Anfodillo, T. & Carraro, V. Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152, 1–12 (2007).
pubmed: 17165095
Utkina, I. A. & Rubtsov, V. V. Studies of phenological forms of pedunculated oak. Contemp. Probl. Ecol. 10, 804–811 (2017).
Seo, J. W., Eckstein, D., Jalkanen, R., Rickebusch, S. & Schmitt, U. Estimating the onset of cambial activity in Scots pine in northern Finland by means of the heat-sum approach. Tree Physiol. 28, 105–112 (2008).
pubmed: 17938119
Zheng, J., Zhao, X., Morris, H. & Jansen, S. Phylogeny best explains latitudinal patterns of xylem tissue fractions for woody angiosperm species across China. Front. Plant Sci. 10, 556 (2019).
pubmed: 31130973
pmcid: 6509232
Swidrak, I., Gruber, A., Kofler, W. & Oberhuber, W. Effects of environmental conditions on onset of xylem growth in Pinus sylvestris under drought. Tree Physiol. 31, 483–493 (2011).
pubmed: 21593011
pmcid: 3427020
Wang, Z., Yang, B., Deslauriers, A. & Bräuning, A. Intra-annual stem radial increment response of Qilian juniper to temperature and precipitation along an altitudinal gradient in northwestern China. Trees 29, 25–34 (2015).
Jyske, T., Mäkinen, H., Kalliokoski, T. & Nöjd, P. Intra-annual tracheid production of Norway spruce and Scots pine across a latitudinal gradient in Finland. Agric. For. Meteorol. 194, 241–254 (2014).
Mäkinen, H., Jyske, T. & Nöjd, P. Dynamics of diameter and height increment of Norway spruce and Scots pine in southern Finland. Ann. For. Sci. 75, 28 (2018).
Prislan, P. et al. Growing season and radial growth predicted for Fagus sylvatica under climate change. Climatic Change 153, 181–197 (2019).
Begum, S. et al. Localized cooling of stems induces latewood formation and cambial dormancy during seasons of active cambium in conifers. Ann. Bot. 117, 465–477 (2016).
pubmed: 26703452
Rahman, M. H. et al. Changes in cambial activity are related to precipitation patterns in four tropical hardwood species grown in Indonesia. Am. J. Bot. 106, 1–12 (2019).
Nakaba, S. et al. Three-dimensional imaging of cambium and secondary xylem cells by confocal laser scanning microscopy. In Plant Microtechniques and Protocols (eds Yeung, E. C. T. et al.) 431–465 (Springer, Heidelberg, 2015).
Kitin, P., Funada, R., Sano, Y. & Ohtani, J. Analysis by confocal microscopy of the structure of cambium in the hardwood Kalopanax pictus. Ann. Bot. 86, 1109–1117 (2000).
Funada, R. Microtubules and the control of wood formation. In Plant Microtubules (ed. Nick, P.) 83–119 (Springer, Heidelberg, 2008).
Begum, S. et al. A rapid decrease in temperature induces latewood formation in artificially reactivated cambium of conifer stems. Ann. Bot. 110, 875–885 (2012).
pubmed: 22843340
pmcid: 3423807
Houtman, C. J., Kitin, P., Houtman, J. C. D., Hammel, K. E. & Hunt, C. G. Acridine orange indicates early oxidation of wood cell walls by fungi. PLoS ONE 11, e0159715 (2016).
pubmed: 27454126
pmcid: 4959780
Hubbe, M. A., Chandra, R. P., Dogu, D. & van Velzen, S. T. G. Analytical staining of cellulosic materials: a review. BioResources 14, 7387–7464 (2019).
Kitin, P., Funada, R., Sano, Y., Beeckman, H. & Ohtani, J. Variations in the lengths of fusiform cambial cells and vessel elements in Kalopanax pictus. Ann. Bot. 84, 621–632 (1999).
Kitin, P., Sano, Y. & Funada, R. Fusiform cells in the cambium of Kalopanax pictus are exclusively mononucleate. J. Exp. Bot. 53, 483–488 (2002).
pubmed: 11847247