The coordinated response of xylem vessels and pits of Fraxinus mandshurica to drought during earlywood and latewood formation

Abstract

The formation of wood is affected by the growing season and the environment. Ring-porous tree species have distinct earlywood-latewood differences. However, it is not clear how earlywood and latewood respond to drought and the differences in adaptation. Therefore, based on the analyses of phenology, growth, and xylem development over a year, xylem development in Fraxinus mandshurica was divided into earlywood, transition, and latewood stages. Variation patterns of 38 wood indices from 31 genotypes indicated that the formation of wood tissues was inhibited, and the proportion of xylem cells was affected by drought at each stage. However, soluble sugar affected osmotic regulation only during drought across earlywood and transition stages. To maintain water and nutrient transport during drought and to resist embolism risk, drought in the earlywood stage leads to varying degrees of earlywood vessel diameter reduction, with pits enlarging to compensate. In contrast, during the latewood stage, drought causes latewood vessel diameter to increase and pits to shrink accordingly. In addition, the results indicate that several wood indices correlate with drought resistance at each stage, but earlywood vessel diameter, soluble sugar, and latewood vessel diameters exhibited the strongest correlations in the earlywood, transition, and latewood stages. These findings provide clues to understanding plant survival strategies under drought stress and are of significance for plant ecology research on the growth and adaptation of tree species under climate change.

Keywords

Drought / Vascular system / Wood development / Ring-porous wood

References

[1] Aliche EB, Prusova-Bourke A, Ruiz-Sanchez M, Oortwijn M, Gerkema E, Van As H, Visser RGF, van der Linden CG. Morphological and physiological responses of the potato stem transport tissues to dehydration stress. Planta, 2020, 251(2): 45

[2] Apuli RP, Richards T, Rendón-Anaya M, Karacic A, Rönnberg-Wästljung AC, Ingvarsson PK. The genetic basis of adaptation in phenology in an introduced population of Black Cottonwood (Populus trichocarpa, Torr. & Gray). BMC Plant Biol, 2021, 21(1 317

[3] Avila RT, Cardoso AA, Batz TA, Kane CN, DaMatta FM, McAdam SAM. Limited plasticity in embolism resistance in response to light in leaves and stems in species with considerable vulnerability segmentation. Physiol Plant, 2021, 172(42142-2152

[4] Ávila-Lovera E, Haro R, Choudhary M, Acosta-Rangel A, Pratt RB, Santiago LS. The benefits of woody plant stem photosynthesis extend to hydraulic function and drought survival in Parkinsonia florida. Tree Physiol, 2024, 44(3 tpae013

[5] Beikircher B, Held M, Losso A, Mayr S. New insights into a sensitive life stage: hydraulics of tree seedlings in their first growing season. New Phytol, 2025, 245(2): 577-590

[6] Blumstein MJ, Furze ME. Interannual dynamics of stemwood nonstructural carbohydrates in temperate forest trees surrounding drought. J Forestry Res, 2023, 34(1): 77-86

[7] Bonasia A, Lazzizera C, Elia A, Conversa G. Nutritional, biophysical and physiological characteristics of wild rocket genotypes as affected by soilless cultivation system, salinity level of nutrient solution and growing period. Front Plant Sci, 2017, 8: 300

[8] Byambadorj SO, Park BB, Hernandez JO, Tsedensodnom E, Byambasuren O, Montagnoli A, Chiatante D, Nyam-Osor B. Effects of irrigation and fertilization on the morphophysiological traits of Populus sibirica hort. ex tausch and Ulmus pumila L. in the semiarid steppe region of Mongolia. Plants, 2021, 10(11 2407

[9] Cai KW, Zhou XY, Li X, Kang Y, Yang XM, Cui YH, Li GY, Pei XN, Zhao XY. Insight into the multiple branches traits of a mutant in Larix olgensis by morphological, cytological, and transcriptional analyses. Front Plant Sci, 2021, 12 787661

[10] Cai HY, Lin Y, Liang YT, Yang G, Sun L. Time since fire affects ecological stoichiometry of plant–soil–microbial systems of Betula platyphylla, a pioneer species in burnt areas of China’s boreal forest. J Forestry Res, 2024, 35(1): 105

[11] Castro VR, Chambi-Legoas R, Filho MT, Surdi PG, Zanuncio JC, Zanuncio AJV. The effect of soil nutrients and moisture during ontogeny on apparent wood density of Eucalyptus grandis. Sci Rep, 2020, 10(12530

[12] Chen YZ, Rademacher T, Fonti P, Eckes-Shephard AH, LeMoine JM, Fonti MV, Richardson AD, Friend AD. Inter-annual and inter-species tree growth explained by phenology of xylogenesis. New Phytol, 2022, 235(3939-952

[13] Christman MA, Sperry JS, Adler FR. Testing the ‘rare pit’ hypothesis for xylem cavitation resistance in three species of Acer. New Phytol, 2009, 182(3664-674

[14] Copini P, Vergeldt FJ, Fonti P, Sass-Klaassen U, den Ouden J, Sterck F, Decuyper M, Gerkema E, Windt CW, Van As H. Magnetic resonance imaging suggests functional role of previous year vessels and fibres in ring-porous sap flow resumption. Tree Physiol, 2019, 39(6): 1009-1018

[15] De Baerdemaeker NJF, Arachchige KNR, Zinkernagel J, Van den Bulcke J, Van Acker J, Schenk HJ, Steppe K. The stability Enigma of hydraulic vulnerability curves: addressing the link between hydraulic conductivity and drought-induced embolism. Tree Physiol, 2019, 39(10): 1646-1664

[16] Depardieu C, Lenz P, Marion J, Nadeau S, Girardin MP, Marchand W, Bégin C, Treydte K, Gessler A, Bousquet J, Savard MM, Isabel N. Contrasting physiological strategies explain heterogeneous responses to severe drought conditions within local populations of a widespread conifer. Sci Total Environ, 2024, 923 171174

[17] Driesen E, De Proft M, Saeys W. Soil moisture levels affect the anatomy and mechanical properties of basil stems (Ocimum basilicum L.). Plants, 2021, 10(7 1320

[18] Epila J, De Baerdemaeker NJF, Vergeynst LL, Maes WH, Beeckman H, Steppe K. Capacitive water release and internal leaf water relocation delay drought-induced cavitation in African Maesopsis eminii. Tree Physiol, 2017, 37(4): 481-490

[19] Espino S, Jochen SH. Mind the bubbles: achieving stable measurements of maximum hydraulic conductivity through woody plant samples. J Exp Bot, 2011, 62(3): 1119-1132

[20] Feng F, Wagner Y, Klein T, Hochberg U. Xylem resistance to cavitation increases during summer in Pinus halepensis. Plant Cell Environ, 2023, 46(6): 1849-1859

[21] Fonti P, Heller O, Cherubini P, Rigling A, Arend M. Wood anatomical responses of oak saplings exposed to air warming and soil drought. Plant Biol, 2013, 15(Suppl 1): 210-219

[22] Friend AD, Eckes-Shephard AH, Tupker Q. Wood structure explained by complex spatial source-sink interactions. Nat Commun, 2022, 13(1): 7824

[23] Furze ME, Huggett BA, Chamberlain CJ, Wieringa MM, Aubrecht DM, Carbone MS, Walker JC, Xu XM, Czimczik CI, Richardson AD. Seasonal fluctuation of nonstructural carbohydrates reveals the metabolic availability of stemwood reserves in temperate trees with contrasting wood anatomy. Tree Physiol, 2020, 40(101355-1365

[24] Galeano E, Thomas BR. Unraveling genetic variation among white spruce families generated through different breeding strategies: heritability, growth, physiology, hormones and gene expression. Front Plant Sci, 2023, 14: 1052425

[25] Gao WQ, Lei XD, Fu LY. Impacts of climate change on the potential forest productivity based on a climate-driven biophysical model in northeastern China. J Forestry Res, 2020, 31(6): 2273-2286

[26] Gao JN, Rossi S, Yang B. Origin of intra-annual density fluctuations in a semi-arid area of northwestern China. Front Plant Sci, 2021, 12 777753

[27] Gebauer R, Urban J, Volařík D, Matoušková M, Vitásek R, Houšková K, Hurt V, Pantová P, Polívková T, Plichta R. Does leaf gas exchange correlate with petiole xylem structural traits in Ulmus laevis seedlings under well-watered and drought stress conditions?. Tree Physiol, 2022, 42(122534-2545

[28] Gong XW, Hao GY. The synergistic effect of hydraulic and thermal impairments accounts for the severe crown damage in Fraxinus mandshurica seedlings following the combined drought-heatwave stress. Sci Total Environ, 2023, 856(Pt 1 159017

[29] González-Melo A, Posada JM, Beauchêne J, Lehnebach R, Levionnois S, Derroire G, Clair B. The links between wood traits and species demography change during tree development in a lowland tropical rainforest. AoB Plants, 2023, 16(1 plad090

[30] Gričar J, Jevšenak J, Hafner P, Prislan P, Ferlan M, Lavrič M, Vodnik D, Eler K. Climatic regulation of leaf and cambial phenology in Quercus pubescens: Their interlinkage and impact on xylem and phloem conduits. Sci Total Environ, 2022, 802 149968

[31] Hajek P, Leuschner C, Hertel D, Delzon S, Schuldt B. Trade-offs between xylem hydraulic properties, wood anatomy and yield in Populus. Tree Physiol, 2014, 34(7): 744-756

[32] Hartmann FP, Rathgeber CBK, Badel É, Fournier M, Moulia B. Modelling the spatial crosstalk between two biochemical signals explains wood formation dynamics and tree-ring structure. J Exp Bot, 2021, 72(5): 1727-1737

[33] Harvey HP, Van Den Driessche R. Nutrition, xylem cavitation and drought resistance in hybrid poplar. Tree Physiol, 1997, 17(10): 647-654

[34] He WQ, Liu HY, Qi Y, Liu F, Zhu XR. Patterns in nonstructural carbohydrate contents at the tree organ level in response to drought duration. Glob Chang Biol, 2020, 26(6): 3627-3638

[35] Huang X, Hou ZL, Ma BL, Zhao H, Jiang ZM, Cai J. Seasonality in embolism resistance and hydraulic capacitance jointly mediate hydraulic safety in branches and leaves of oriental cork oak (Quercus variabilis Bl.). Tree Physiol, 2024, 44(9 tpae109

[36] Huo JQ, Li CY, Zhao Y, Han GL, Li XR, Zhang ZS. Hydraulic mechanism of limiting growth and maintaining survival of desert shrubs in arid habitats. Plant Physiol, 2024, 196(4): 2450-2462

[37] Isasa E, Link RM, Jansen S, Tezeh FR, Kaack L, Sarmento Cabral J, Schuldt B. Addressing controversies in the xylem embolism resistance-vessel diameter relationship. New Phytol, 2023, 238(1): 283-296

[38] Jupa R, Rosell JA, Pittermann J. Bark structure is coordinated with xylem hydraulic properties in branches of five Cupressaceae species. Plant Cell Environ, 2024, 47(5): 1439-1451

[39] Kaack L, Weber M, Isasa E, Karimi Z, Li S, Pereira L, Trabi CL, Zhang Y, Jochen Schenk H, Schuldt B, Schmidt V, Jansen S. Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms. New Phytol, 2021, 230(5): 1829-1843

[40] Keret R, Drew DM, Hills PN. Xylem cell size regulation is a key adaptive response to water deficit in Eucalyptus grandis. Tree Physiol, 2024, 44(7 tpae068

[41] Lenka SK, Katiyar A, Chinnusamy V, Bansal KC. Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnol J, 2011, 9(3): 315-327

[42] Levionnois S, Jansen S, Wandji RT, Beauchêne J, Ziegler C, Coste S, Stahl C, Delzon S, Authier L, Heuret P. Linking drought-induced xylem embolism resistance to wood anatomical traits in Neotropical trees. New Phytol, 2021, 229(3): 1453-1466

[43] Li JM, Wei J, Liu YC, Liu B, Liu T, Jiang Y, Ding LQ, Liu C. A microfluidic design to provide a stable and uniform in vitro microenvironment for cell culture inspired by the redundancy characteristic of leaf areoles. Lab Chip, 2017, 17(22): 3921-3933

[44] Li MJ, Wang L, Zhang J, Zhan RL, An NN, Sun YD, Wu FL, Yang JJ, Su HY, Cochard H, Jiang XM, Shu JH, Zheng JM, Yin YF. Single-walled carbon nanotubes promotes wood formation in Populus davidiana × P.bolleana .. Plant physiology and biochemistry, 2022, 184: 137-143

[45] Li ZM, Luo DD, Ibrahim MM, Luo XZ, Deng RF, Wang CK, Hou EQ. Seasonal changes in hydraulic functions of eight temperate tree species: divergent responses to freeze-thaw cycles in spring and autumn. Tree Physiol, 2024, 44(11 tpae132

[46] Licaj I, Germinario C, Di Meo MC, Varricchio E, Rocco M. The physiology and anatomy study in leaves of Saragolla and Svevo wheat cultivars under polyethylene glycol-simulated drought stress. Funct Plant Biol, 2024, 51 FP23151

[47] Liu YY, Song J, Wang M, Li N, Niu CY, Hao GY. Coordination of xylem hydraulics and stomatal regulation in keeping the integrity of xylem water transport in shoots of two compound-leaved tree species. Tree Physiol, 2015, 35(12): 1333-1342

[48] Long JL, Xing W, Wang YG, Wu ZD, Li WJ, Zou Y, Sun JP, Zhang FS, Pi Z. Comparative proteomic analysis on chloroplast proteins provides new insights into the effects of low temperature in sugar beet. Bot Stud (Taipei), 2022, 63(1): 18

[49] Lu H, Chen MJ, Fu M, Yan JL, Su WL, Zhan YG, Zeng FS. Brassinosteroids affect wood development and properties of Fraxinus mandshurica. Front Plant Sci, 2023, 14: 1167548

[50] Marchand LJ, Dox I, Gričar J, Prislan P, Van den Bulcke J, Fonti P, Campioli M. Timing of spring xylogenesis in temperate deciduous tree species relates to tree growth characteristics and previous autumn phenology. Tree Physiol, 2021, 41(71161-1170

[51] Marchin RM, Backes D, Ossola A, Leishman MR, Tjoelker MG, Ellsworth DS. Extreme heat increases stomatal conductance and drought-induced mortality risk in vulnerable plant species. Glob Chang Biol, 2022, 28(31133-1146

[52] Mekarni L, Cochard H, Lehmann MM, Turberg P, Grossiord C. In vivo X-ray microtomography locally affects stem radial growth with no immediate physiological impact. Plant Physiol, 2024, 196(1): 153-163

[53] Namvar S, Boucher É, Deslauriers A, Morin H, Savard MM. Monitoring weekly δ¹³C variations along the cambium-xylem continuum in the Canadian eastern boreal forest. Tree Physiol, 2024, 44(11 tpae136

[54] Noyer E, Stojanović M, Horáček P, Pérez-de-Lis G. Toward a better understanding of angiosperm xylogenesis: a new method for a cellular approach. New Phytol, 2023, 239(2): 792-805

[55] Ouyang WQ, Chen LM, Ma JK, Liu XR, Chen HF, Yang HL, Guo W, Shan ZH, Yang ZL, Chen SL, Zhan Y, Zhang HB, Cao D, Zhou XN. Identification of quantitative trait locus and candidate genes for drought tolerance in a soybean recombinant inbred line population. Int J Mol Sci, 2022, 23(18): 10828

[56] Paiva FJDS, Lima GS, Lima VLA, Souza WBB, Soares LADA, Torres RAF, Gheyi HR, Silva LA, Sá FVDS, Sá VKNO, Silva STA, Fátima RT, Fernandes PD, Almeida AKC. The effects of irrigation water salinity on the synthesis of photosynthetic pigments, gas exchange, and photochemical efficiency of sour passion fruit genotypes. Plants, 2023, 12(223894

[57] Pereira L, Kaack L, Guan XY, de Melo SL, Miranda MT, Pires GS, Ribeiro RV, Schenk HJ, Jansen S. Angiosperms follow a convex trade-off to optimize hydraulic safety and efficiency. New Phytol, 2023, 240(51788-1801

[58] Pérez-de-Lis G, Rossi S, Vázquez-Ruiz RA, Rozas V, García-González I. Do changes in spring phenology affect earlywood vessels?Perspective from the xylogenesis monitoring of two sympatric ring-porous oaks. New Phytol, 2016, 209(2): 521-530

[59] Płachno BJ, Kapusta M. The localization of cell wall components in the quadrifids of whole-mount immunolabeled Utricularia dichotoma traps. Int J Mol Sci, 2023, 25(1): 56

[60] Pompa-García M, Julio Camarero J, Valeriano C, Vivar-Vivar ED. Climate sensitivity of seasonal radial growth in young stands of Mexican conifers. Int J Biometeorol, 2022, 66(81711-1723

[61] Pradhan D, Bertin D, Sinclair TR, Nogueira MA, Livingston D, Carter T. Microsphere stem blockage as a screen for nitrogen-fixation drought tolerance in soybean. Physiol Plant, 2021, 172(2): 1376-1381

[62] Pratt RB, Jacobsen AL, Percolla MI, De Guzman ME, Traugh CA, Tobin MF. Trade-offs among transport, support, and storage in xylem from shrubs in a semiarid chaparral environment tested with structural equation modeling. Proc Natl Acad Sci USA, 2021, 118(33 e2104336118

[63] Pritzkow C, Brown MJM, Carins-Murphy MR, Bourbia I, Mitchell PJ, Brodersen C, Choat B, Brodribb TJ. Conduit position and connectivity affect the likelihood of xylem embolism during natural drought in evergreen woodland species. Ann Bot, 2022, 130(3): 431-444

[64] Ranjan R, Khurana R, Malik N, Badoni S, Parida SK, Kapoor S, Tyagi AK. bHLH142 regulates various metabolic pathway-related genes to affect pollen development and anther dehiscence in rice. Sci Rep, 2017, 7: 43397

[65] Rauschendorfer J, Rooney R, Külheim C. Strategies to mitigate shifts in red oak (Quercus sect. Lobatae) distribution under a changing climate. Tree Physiol, 2022, 42(12): 2383-2400

[66] Rita A, Pericolo O, Tumajer J, Ripullone F, Gentilesca T, Saracino A, Borghetti M. Tip-to-base conduit widening remains consistent across cambial age and climates in Fagus sylvatica L. Tree Physiol, 2024, 44(7 tpae080

[67] Rodríguez-Ramírez EC, Eugenia Ferrero M, Acevedo-Vega I, Crispin-DelaCruz DB, Ticse-Otarola G, Requena-Rojas EJ. Plastic adjustments in xylem vessel traits to drought events in three Cedrela species from Peruvian Tropical Andean forests. Sci Rep, 2022, 12(121112

[68] Rossi S, Morin H, Deslauriers A. Causes and correlations in cambium phenology: towards an integrated framework of xylogenesis. J Exp Bot, 2012, 63(52117-2126

[69] Song YJ, Poorter L, Horsting A, Delzon S, Sterck F. Pit and tracheid anatomy explain hydraulic safety but not hydraulic efficiency of 28 conifer species. J Exp Bot, 2022, 73(3): 1033-1048

[70] Sorek Y, Greenstein S, Netzer Y, Shtein I, Jansen S, Hochberg U. An increase in xylem embolism resistance of grapevine leaves during the growing season is coordinated with stomatal regulation, turgor loss point and intervessel pit membranes. New Phytol, 2021, 229(4): 1955-1969

[71] Sorek Y, Netzer Y, Cohen S, Hochberg U. Rapid leaf xylem acclimation diminishes the chances of embolism in grapevines. J Exp Bot, 2023, 74(21): 6836-6846

[72] Stefaniak EZ, Tissue DT, Dewar RC, Medlyn BE. Optimal carbon storage during drought. Tree Physiol, 2024, 44(13): 34-45

[73] Tomasella M, Casolo V, Natale S, Petruzzellis F, Kofler W, Beikircher B, Mayr S, Nardini A. Shade-induced reduction of stem nonstructural carbohydrates increases xylem vulnerability to embolism and impedes hydraulic recovery in Populus nigra. New Phytol, 2021, 231(1): 108-121

[74] Uggla C, Magel E, Moritz T, Sundberg B. Function and dynamics of auxin and carbohydrates during earlywood/latewood transition in Scots pine. Plant Physiol, 2001, 125(4): 2029-2039

[75] Vaz M, Pereira JS, Gazarini LC, David TS, David JS, Rodrigues A, Maroco J, Chaves MM. Drought-induced photosynthetic inhibition and autumn recovery in two Mediterranean oak species (Quercus ilex and Quercus suber). Tree Physiol, 2010, 30(8): 946-956

[76] Wang GY, Ahmad S, Wang Y, Wang BW, Huang JH, Jahan MS, Zhou XB, Shi CQ. Multivariate analysis compares and evaluates drought and flooding tolerances of maize germplasm. Plant Physiol, 2023, 193(1): 339-355

[77] Wang XN, Xu TR, Xu CX, Liu HY, Chen ZJ, Li ZS, Li XM, Wu XC. Enhanced growth resistance but no decline in growth resilience under long-term extreme droughts. Glob Change Biol, 2024, 30(1 e17038

[78] Wang AY, Li SQ, Cui HX, Liu YN, Lu YJ, Hao GY. Divergence in leaf and cambium phenologies among three temperate tree species of different wood types with special reference to xylem hydraulics. Front Plant Sci, 2025, 16: 1562873

[79] Wason J, Bouda M, Lee EF, McElrone AJ, Phillips RJ, Shackel KA, Matthews MA, Brodersen C. Xylem network connectivity and embolism spread in grapevine (Vitis vinifera L.). Plant Physiol, 2021, 186(1): 373-387

[80] Wildhagen H, Paul S, Allwright M, Smith HK, Malinowska M, Schnabel SK, João Paulo M, Cattonaro F, Vendramin V, Scalabrin S, Janz D, Douthe C, Brendel O, Buré C, Cohen D, Hummel I, Le Thiec D, van Eeuwijk F, Keurentjes JJB, Flexas J, Morgante M, Robson P, Bogeat-Triboulot MB, Taylor G, Polle A. Genes and gene clusters related to genotype and drought-induced variation in saccharification potential, lignin content and wood anatomical traits in Populus nigra. Tree Physiol, 2018, 38(3320-339

[81] Yan CJ, Song SH, Wang WB, Wang CL, Li HB, Wang F, Li SY, Sun XG. Screening diverse soybean genotypes for drought tolerance by membership function value based on multiple traits and drought-tolerant coefficient of yield. BMC Plant Biol, 2020, 20(1): 321

[82] Zahnd C, Zehnder M, Arend M, Kahmen A, Hoch G. Uniform carbon reserve dynamics along the vertical light gradient in mature tree crowns. Tree Physiol, 2024, 44(13232-245

[83] Zarrinderakht M, Konrad I, Wilmot TR, Perkins TD, van den Berg AK, Stockie JM. Experimental and computational comparison of freeze-thaw-induced pressure generation in red and sugar maple. Tree Physiol, 2024, 44(4): tpae006

[84] Zhang X, Fan ZF, Shi ZJ, Pan LL, Kwon S, Yang XH, Liu YS. Tree characteristics and drought severity modulate the growth resilience of natural Mongolian pine to extreme drought episodes. Sci Total Environ, 2022, 830 154742

[85] Zhang YX, Wang XC, Zhang R, Niu AL, Wang CK, Jin Y. Impacts of short-term rainfall and snowfall exclusions on hydraulic, economic and stomatal traits of Larix gmelinii in northeastern China. J Forestry Res, 2024, 35(1137

[86] Zhang XL, Ma SW, Hu H, Li FL, Bao WK, Huang L. A trade-off between leaf hydraulic efficiency and safety across three xerophytic species in response to increased rock fragment content. Tree Physiol, 2025, 44(3tpae10

[87] Zhao H, Huang X, Ma BL, Jiang B, Jiang ZM, Cai J. Productive poplar genotypes exhibited temporally stable low stem embolism resistance and hydraulic resistance segmentation at the stem-leaf transition. Plant Cell Environ, 2025, 48(2992-1004

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