Intra-seasonal trends in phloem traits in Pinus spp. from drought-prone environments

In: IAWA Journal

Abstract

Recent studies on the seasonal dynamics of secondary tissue formation in Mediterranean trees have shown that xylogenesis depends on species and site conditions, but many questions still remain open. On the other side of the cambium, even less information is available about phloem structure and timing of its formation. We analysed intra-annual phloem variation in width and cell traits in the conducting, non-collapsed phloem (CPH) of Pinus pinea and Pinus halepensis at Mediterranean sites in southern Italy and Spain. In all investigated trees, it was possible to differentiate among the non-conducting, collapsed phloem (NCPH), and the CPH. CPH showed no evident annual growth layers; no differences in radial dimensions of early- and late phloem sieve cells, and no cyclic patterns of axial parenchyma distribution. Since it was not possible to study the seasonality of the phloem growth, we analysed the entire CPH. CPH width showed seasonal fluctuations and was generally the widest during the maximum cambial activity and narrowest during summer and winter. The radial size of newly formed sieve cells varied in relation to seasonal dynamics of cambial activity and fluctuations in local weather conditions. The number of axial parenchyma cells in CPH increased during the summer. The observed intra-annual variations in CPH width and structure seemed to be correlated with seasonal weather conditions in order to ensure a sufficient amount of conducting phloem tissue for translocation of photosynthates and signalling molecules to the actively growing tissues along the stem of a tree growing in the harsh Mediterranean conditions.

  • Adler PBSalguero-Gómez RCompagnoni AHsu JSRay-Mukherjee JMbeau-Ache CFranco M. 2014. Functional traits explain variation in plant life history strategies. Proc. Natl. Acad. Sci. 2: 740745. DOI: 10.1073/pnas.1315179111.

    • Search Google Scholar
    • Export Citation
  • Alfieri FJEvert RF. 1968. Seasonal development of the secondary phloem in Pinus. Am. J. Bot. 55: 518528.

  • Anderegg WRKlein TBartlett MSack LPellegrini AFChoat BJansen S. 2016. Met-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proc. Natl. Acad. Sci. 18: 50245029. DOI: 10.5061/dryad.116j2.

    • Search Google Scholar
    • Export Citation
  • Angyalossy VPace MREvert RFMarcati CROskolski AAet al. 2016. IAWA list of microscopic bark features. IAWA J. 37: 517615. DOI: 10.1163/22941932-20160151.

    • Search Google Scholar
    • Export Citation
  • Awada TRadoglou KFotelli MNConstantinidou HI. 2003. Ecophysiology of seedlings of three Mediterranean pine species in contrasting light regimes. Tree Physiol. 23: 3341. DOI: 10.1093/treephys/23.1.33.

    • Search Google Scholar
    • Export Citation
  • Baas PMiller RB. 1985. Functional and ecological wood anatomy some introductory comments. IAWA J. 6: 281282. DOI: 10.1163/22941932-90000955.

    • Search Google Scholar
    • Export Citation
  • Balzano ABattipaglia GDe Micco V. 2019a. Wood-trait analysis to understand climatic factors triggering intra-annual density fluctuations in co-occurring Mediterranean trees. IAWA J. 40: 241258. DOI: 10.1163/22941932-40190220.

    • Search Google Scholar
    • Export Citation
  • Balzano AČufar KBattipaglia GMerela MPrislan PAronne GDe Micco V. 2018. Xylogenesis reveals the genesis and ecological signal of IADFs in Pinus pinea L. and Arbutus unedo L. Ann. Bot. 121: 12311242. DOI: 10.1093/aob/mcy008.

    • Search Google Scholar
    • Export Citation
  • Balzano ADe Micco VMerela MČufar K. 2019b. Tree rings in Mediterranean pines — can we ascribe them to calendar years? Les/Wood 68: 514. DOI: 10.26614/les-wood.2019.v68n01a01.

    • Search Google Scholar
    • Export Citation
  • Barnett J. 1971. Winter activity in the cambium of Pinus radiata. NZ J. For. Res. 1: 208222.

  • Battipaglia GDe Micco VSass-Klaassen UTognetti RMäkelä A. 2014a. Special issue: WSE symposium: wood growth under environmental changes: the need for a multidisciplinary approach. Tree Physiol. 34: 787791. DOI: 10.1093/treephys/tpu076.

    • Search Google Scholar
    • Export Citation
  • Battipaglia GDe Micco VBrand WASaurer MAronne GLinke PCherubini P. 2014b. Drought impact on water use efficiency and intra-annual density fluctuations in Erica arborea on Elba Italy. Plant Cell Environ. 37: 382391. DOI: 10.1111/pce.12160.

    • Search Google Scholar
    • Export Citation
  • Beeckman H. 2016. Wood anatomy and trait-based ecology. IAWA J. 37: 127151. DOI: 10.1163/22941932-20160127.

  • Brodribb TJMcAdam SAJordan GJMartins SC. 2014. Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proc. Natl. Acad. Sci. USA 111: 1448914493. DOI: 10.1073/pnas.1407930111.

    • Search Google Scholar
    • Export Citation
  • Campelo FNabais CGutiérrez EFreitas HGarcía-González I. 2010. Vessel features of Quercus ilex L. growing under Mediterranean climate have a better climatic signal than tree-ring width. Trees 24: 463470. DOI: 10.1007/s00468-010-0414-0.

    • Search Google Scholar
    • Export Citation
  • Čufar KPrislan Pde Luis MGričar J. 2008. Tree-ring variation, wood formation and phenology of beech (Fagus sylvatica) from a representative site in Slovenia, SE central Europe. Trees 22: 749758. DOI: 10.1007/s00468-008-0235-6.

    • Search Google Scholar
    • Export Citation
  • de Luis MGričar JČufar KRaventós J. 2007. Seasonal dynamics of wood formation in Pinus halepensis from dry and semi-arid ecosystems in Spain. IAWA J. 28: 389404. DOI: 10.1163/22941932-90001651.

    • Search Google Scholar
    • Export Citation
  • de Luis MNovak KRaventós JGričar JPrislan PČufar K. 2011. Climate factors promoting intra-annual density fluctuations in Aleppo pine (Pinus halepensis) from semiarid sites. Dendrochronologia 29: 163169. DOI: 10.1016/j.dendro.2011.01.005.

    • Search Google Scholar
    • Export Citation
  • De Micco VAronne GBaas P. 2008. Wood anatomy and hydraulic architecture of stems and twigs of some Mediterranean trees and shrubs along a mesic-xeric gradient. Trees 22: 643655. DOI: 10.1007/s00468-008-0222-y.

    • Search Google Scholar
    • Export Citation
  • De Micco VBalzano AČufar KAronne GGričar JMerela MBattipaglia G. 2016a. Timing of false ring formation in Pinus halepensis and Arbutus unedo in southern Italy: outlook from an analysis of xylogenesis and tree-ring chronologies. Front. Plant Sci. 7: 705. DOI: 10.3389/fpls.2016.00705.

    • Search Google Scholar
    • Export Citation
  • De Micco VBattipaglia GBalzano ACherubini PAronne G. 2016b. Are wood fibres as sensitive to environmental conditions as vessels in tree rings with intra-annual density fluctuations (IADFs) in Mediterranean species? Trees 30: 971983. DOI: 10.1007/s00468-015-1338-5.

    • Search Google Scholar
    • Export Citation
  • De Micco VCampelo Fde Luis MBräuning AGrabner MBattipaglia GCherubini P. 2016c. Intra-annual density fluctuations in tree rings: how, when, where, and why? IAWA J. 37: 232259. DOI: 10.1163/22941932-20160132.

    • Search Google Scholar
    • Export Citation
  • De Micco VCarrer MRathgeber CBKCamarero JJVoltas JCherubini PBattipaglia G. 2019. From xylogenesis to tree rings: wood traits to investigate tree response to environmental changes. IAWA J. 40: 155182. DOI: 10.1163/22941932-40190246.

    • Search Google Scholar
    • Export Citation
  • Esau K. 1969. The phloem. Encyclopedia of plant anatomy, vol. 5. BornträgerBerlin, Germany.

  • Fry DJPhillips IDJ. 1977. Photosynthesis of conifers in relation to annual growth cycles and dry matter production: II. Seasonal photosynthetic capacity and mesophyll ultrastructure in Abies grandis, Picea sitchensis, Tsuga heterophylla and Larix leptolepis growing in SW England. Physiol. Plantarum 40: 300306. DOI: 10.1111/j.1399-3054.1977.tb04077.x.

    • Search Google Scholar
    • Export Citation
  • García-González IFonti P. 2006. Selecting earlywood vessels to maximize their environmental signal. Tree Physiol. 26: 12891296. DOI: 10.1093/treephys/26.10.1289.

    • Search Google Scholar
    • Export Citation
  • Gea-Izquierdo GViguera BCabrera MCañellas I. 2014. Drought-induced decline could portend widespread pine mortality at the xeric ecotone in managed Mediterranean pine-oak woodlands. For. Ecol. Manag. 320: 7082. DOI: 10.1016/j.foreco.2014.02.025.

    • Search Google Scholar
    • Export Citation
  • Gričar JČufar K. 2008. Seasonal dynamics of phloem and xylem formation in silver fir and Norway spruce as affected by drought. Russ J Plant Physiol. 55: 538543. DOI: 10.1134/S102144370804016X.

    • Search Google Scholar
    • Export Citation
  • Gričar JČufar KOven PSchmitt U. 2005. Differentiation of terminal latewood tracheids in silver fir trees during autumn. Ann. Bot. 95: 959965. DOI: 10.1093/aob/mci112.

    • Search Google Scholar
    • Export Citation
  • Gričar JKrže LČufar K. 2009. Number of cells in xylem, phloem and dormant cambium in silver fir (Abies alba): in trees of different vitality. IAWA J. 30: 121133. DOI: 10.1163/22941932-90000208.

    • Search Google Scholar
    • Export Citation
  • Gričar JPrislan Pde Luis MGryc VHacurová JVavrčík HČufar K. 2015. Plasticity in variation of xylem and phloem cell characteristics of Norway spruce under different local conditions. Front. Plant Sci. 6: 730. DOI: 10.3389/fpls.2015.00730.

    • Search Google Scholar
    • Export Citation
  • Gričar JPrislan Pde Luis MNovak KLongares LAMartinez del Castillo EMČufar K. 2016. Lack of annual periodicity in cambial production of phloem in trees from Mediterranean areas. IAWA J. 37: 349364. DOI: 10.1163/22941932-20160138.

    • Search Google Scholar
    • Export Citation
  • Gričar JZupančič MČufar KOven P. 2007. Regular cambial activity and xylem and phloem formation in locally heated and cooled stem portions of Norway spruce. Wood Sci. Technol. 41: 463475. DOI: 10.1007/s00226-006-0109-2.

    • Search Google Scholar
    • Export Citation
  • Harris IPDJJones PDOsborn TJLister DH. 2014. Updated high-resolution grids of monthly climatic observations — the CRU TS3. 10 dataset. Int. J. Climatol. 34: 623642. DOI: 10.1002/joc.3711.

    • Search Google Scholar
    • Export Citation
  • Holdheide W. 1951. Anatomie mitteleuropäischer Gehölzrinden mit mikrophotographischem Atlas. In: H. Freund Handbuch der Mikroskopie in der Technik 5: 193367.

    • Search Google Scholar
    • Export Citation
  • Hölttä TMäkinen HNöjd PMäkelä ANikinmaa E. 2010. A physiological model of softwood cambial growth. Tree Physiol. 30: 12351252. DOI: 10.1093/treephys/tpq068.

    • Search Google Scholar
    • Export Citation
  • Jyske THölttä T. 2015. Comparison of phloem and xylem hydraulic architecture in Picea abies stems. New Phytol. 205: 102115. DOI: 10.1111/nph.12973.

    • Search Google Scholar
    • Export Citation
  • Jyske TMSuuronen JPPranovich AVLaakso TWatanabe UKuroda KAbe H. 2015. Seasonal variation in formation, structure, and chemical properties of phloem in Picea abies as studied by novel microtechniques. Planta 242: 613629. DOI: 10.1007/s00425-015-2347-8.

    • Search Google Scholar
    • Export Citation
  • Liesche JPace MRXu QLi YChen S. 2017. Height-related scaling of phloem anatomy and the evolution of sieve element end wall types in woody plants. New Phytol. 214: 245256. DOI: 10.1111/nph.14360.

    • Search Google Scholar
    • Export Citation
  • Liphschitz NLev-Yadun SRosen EWaisel Y. 1984. The annual rhythm of activity of the lateral meristems cambium and phellogen in Pinus halepensis mill. and Pinus pinea l. IAWA J. 5: 263274. DOI: 10.1163/22941932-90000413.

    • Search Google Scholar
    • Export Citation
  • McDowell NPockman WTAllen CDBreshears DDCobb NKolb TPlaut JSperry JWest AWilliams DGYepez EA. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 178: 719739. DOI: 10.1111/j.1469-8137.2008.02436.x.

    • Search Google Scholar
    • Export Citation
  • Miyazawa YKikuzawa K. 2005. Winter photosynthesis by saplings of evergreen broadleaved trees in a deciduous temperate forest. New Phytol. 165: 857866. DOI: 10.1111/j.1469-8137.2004.01265.x.

    • Search Google Scholar
    • Export Citation
  • Mullendore DLWindt CWVan As HKnoblauch M. 2010. Sieve tube geometry in relation to phloem flow. Plant Cell. 22: 579593. DOI: 10.1105/tpc.109.070094.

    • Search Google Scholar
    • Export Citation
  • Nanayakkara BDickson ARMeason DF. 2019. Xylogenesis of Pinus radiata D. Don growing in New Zealand. Ann. Forest Sci. 76(3): 74. DOI: 10.1007/s13595-019-0859-2.

    • Search Google Scholar
    • Export Citation
  • Novak Kde Luis MGričar JPrislan PMerela MSmith KTČufar K. 2016a. Missing and dark rings associated with drought in Pinus halepensis. IAWA J. 37: 260274. DOI: 10.1163/22941932-20160133.

    • Search Google Scholar
    • Export Citation
  • Pacheco ACamarero JJCarrer M. 2016. Linking wood anatomy and xylogenesis allows pinpointing of climate and drought influences on growth of coexisting conifers in continental Mediterranean climate. Tree Physiol. 36: 502512. DOI: 10.1093/treephys/tpv125.

    • Search Google Scholar
    • Export Citation
  • Pfautsch SRenard JTjoelker MGSalih A. 2015. Phloem as capacitor: radial transfer of water into xylem of tree stems occurs via symplastic transport in ray parenchyma. Plant Physiol. 167: 963971. DOI: 10.1104/pp.114.254581.

    • Search Google Scholar
    • Export Citation
  • Prislan PGričar Jde Luis MNovak KMartinez del Castillo ESchmitt UKoch GŠtrus JMrak PŽnidarič MTČufar K. 2016. Annual cambial rhythm in Pinus halepensis and Pinus sylvestris as indicator for climate adaptation. Front Plant Sci. 7: 1923. DOI: 10.3389/fpls.2016.01923.

    • Search Google Scholar
    • Export Citation
  • Prislan PMrak PŽnidaršič NŠtrus JHumar MThaler NMrak TGričar J. 2018. Intra-annual dynamics of phloem formation and ultrastructural changes in sieve tubes in Fagus sylvatica. Tree Physiol. 39: 262274. DOI: 10.1093/treephys/tpy102.

    • Search Google Scholar
    • Export Citation
  • Prislan PSchmitt UKoch GGričar JČufar K. 2012. Cellular and topochemical characteristics of secondary changes in bark tissues of beech (Fagus sylvatica). Holzforschung 66: 131138. DOI: 10.1515/HF.2011.119.

    • Search Google Scholar
    • Export Citation
  • Rosell JACastorena MLaws CAWestoby M. 2015. Bark ecology of twigs vs. main stems: functional traits across eighty-five species of angiosperms. Oecologia 178: 10331043. DOI: 10.1007/s00442-015-3307-5.

    • Search Google Scholar
    • Export Citation
  • Rosell JAOlson ME. 2014. The evolution of bark mechanics and storage across habitats in a clade of tropical trees. Am. J. Bot. 101: 764777. DOI: 10.3732/ajb.1400109.

    • Search Google Scholar
    • Export Citation
  • Rossi SAnfodillo TMenardi R. 2006b. Trephor: a new tool for sampling microcores from tree stems. IAWA J. 27: 8997. DOI: 10.1163/22941932-90000139.

    • Search Google Scholar
    • Export Citation
  • Rossi SDeslauriers AAnfodillo TMorin HSaracino AMotta RBorghetti M. 2006a. Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytol. 170: 301310. DOI: 10.1111/j.1469-8137.2006.01660.x.

    • Search Google Scholar
    • Export Citation
  • Rossi SDeslauriers AGričar JSeo J-WRathgeber CBKAnfodillo TMorin HLevanic TOven PJalkanen R. 2008. Critical temperatures for xylogenesis in conifers of cold climates. Glob. Ecol. Biogeogr. 17: 696707. DOI: 10.1111/j.1466-8238.2008.00417.x.

    • Search Google Scholar
    • Export Citation
  • Secchi FPagliarani CZwieniecki MA. 2017. The functional role of xylem parenchyma cells and aquaporins during recovery from severe water stress. Plant Cell Environ. 40: 858871. DOI: 10.1111/pce.12831.

    • Search Google Scholar
    • Export Citation
  • Sterck FJPoorter LSchieving F. 2006. Leaf traits determine the growth-survival trade-off across rain forest tree species. Am. Nat. 167: 758765. DOI: 10.1086/503056.

    • Search Google Scholar
    • Export Citation
  • Taiz LZeiger E. 2006. Plant physiology4th Edn. Sinauer Associates, Inc.Sunderland.

  • Trockenbrodt M. 1990. Survey and discussion of the terminology used in bark anatomy. IAWA J. 11: 141166. DOI: 10.1163/22941932-90000511.

    • Search Google Scholar
    • Export Citation
  • Troeng ELinder S. 1982. Gas exchange in a 20-year-old stand of Scots pine: II. Variation in net photosynthesis and transpiration within and between trees. Physiol. Plantarum 54: 1523. DOI: 10.1111/j.1399-3054.1982.tb00570.x.

    • Search Google Scholar
    • Export Citation
  • Verheyden AHelle GSchleser GHDehairs FBeeckman HKoedam N. 2004. Annual cyclicity in high-resolution stable carbon and oxygen isotope ratios in the wood of the mangrove tree Rhizophora mucronata. Plant Cell Environ. 27: 15251536. DOI: 10.1111/j.1365-3040.2004.01258.x.

    • Search Google Scholar
    • Export Citation
  • Zalloni EBattipaglia GCherubini PDe Micco V. 2018a. Site conditions influence the climate signal of intra-annual density fluctuations in tree rings of Q. ilex L. Ann. For. Sci. 75: 68. DOI: 10.1007/s13595-018-0748-0.

    • Search Google Scholar
    • Export Citation
  • Zalloni Ede Luis MCampelo FNovak KDe Micco VDi Filippo AVieira JNabais CRozas VBattipaglia G. 2016. Climatic signals from intra-annual density fluctuation frequency in Mediterranean pines at a regional scale. Front Plant Sci. 7: 579. DOI: 10.3389/fpls.2016.00579.

    • Search Google Scholar
    • Export Citation
  • Ziaco EBiondi FHeinrich I. 2016. Wood cellular dendroclimatology: testing new proxies in Great Basin bristlecone pine. Front Plant Sci. 7: 1602. DOI: 10.3389/fpls.2016.01602.

    • Search Google Scholar
    • Export Citation

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