Root grafts matter for inter-tree water exchange - a quantification of water translocation between root grafted mangrove trees using field data and model based indication

. 2022 Jun 10 ; 130 (3) : 317-30. [epub] 20220610

Status Publisher Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35686514

BACKGROUND AND AIMS: Trees interconnected through functional root grafts can exchange resources, but the effect of exchange on trees remains under debate. A mechanistic understanding of resources exchange via functional root grafts will help understand their ecological implications for tree water exchange for individual trees, groups of trees, and forest stands. METHODS: To identify the main patterns qualitatively describing the movement of sap between grafted trees, we reviewed available literature on root grafting in woody plants that focus on tree allometry and resource translocation via root grafts. We then extended the BETTINA model, which simulates mangrove (Avicennia germinans) tree growth on the individual tree scale, in order to synthesize the available empirical information. Using allometric data from a field study in mangrove stands, we simulated potential water exchange and analyzed movement patterns between grafted trees. KEY RESULTS: In the simulations, relative water exchange ranged between -9.17 and 20.3 %, and was driven by gradients of water potential, i.e. differences in tree size and water availability. Moreover, the exchange of water through root grafts alters the water balance of trees and their feedback with the soil: grafted trees that receive water from their neighbors reduce their water uptake. CONCLUSIONS: Our individual-tree modelling study is a first theoretical attempt to quantify root graft-mediated water exchange between trees. Our findings indicate that functional root grafts represent a vector of hydraulic redistribution, helping to maintain the water balance of grafted trees. This non-invasive approach can serve as a fundament for designing empirical studies to better understand the role of grafted root interaction networks on a broader scale.

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Adonsou KE, Desrochers A, Tremblay F.. 2016a. Physiological integration of connected balsam poplar ramets. Tree Physiology 36: 797–806. doi:10.1093/treephys/tpv142. PubMed DOI

Adonsou KE, Drobyshev I, DesRochers A, Tremblay F.. 2016b. Root connections affect radial growth of balsam poplar trees. Trees 30: 1775–1783. doi:10.1007/s00468-016-1409-2. DOI

Appel DN. 1994. Identification and control of oak wilt in Texas urban forests. Journal of Arboriculture 20: 250–258.

Bader MK-F, Leuzinger S.. 2019. Hydraulic coupling of a leafless kauri tree remnant to conspecific hosts. iScience 19: 1238–1247. doi:10.1016/j.isci.2019.05.009. PubMed DOI PMC

Ball MC, Farquhar GD.. 1984. Photosynthetic and stomatal responses of two Mangrove species, Aegiceras corniculatum and Avicennia marina, to long term salinity and humidity conditions. Plant Physiology 74: 1–6. doi:10.1104/pp.74.1.1. PubMed DOI PMC

Baret M, DesRochers A.. 2011. Root connections can trigger physiological responses to defoliation in nondefoliated aspen suckers. Botany 89: 753–761. doi:10.1139/b11-062. DOI

Baric S, Kerschbamer C, Vigl J, Dalla Via J.. 2008. Translocation of apple proliferation phytoplasma via natural root grafts – a case study. European Journal of Plant Pathology 121: 207–211.

Basnet K, Scatena FN, Likens GE, Lugo AE.. 1993. Ecological consequences of root grafting in Tabonuco (Dacryodes excelsa) trees in the Luquillo Experimental Forest, Puerto Rico. Biotropica 25: 28–35. doi:10.2307/2388976. DOI

Bathmann J, Peters R, Naumov D, Fischer T, Berger U, Walther M.. 2020. The MANgrove–GroundwAter feedback model (MANGA) – describing belowground competition based on first principles. Ecological Modelling 420: 108973. doi:10.1016/j.ecolmodel.2020.108973. DOI

Bathmann J, Peters R, Reef R, Berger U, Walther M, Lovelock CE.. 2021. Modelling mangrove forest structure and species composition over tidal inundation gradients: the feedback between plant water use and porewater salinity in an arid mangrove ecosystem. Agricultural and Forest Meteorology 308–309: 108547.

Bazihizina N, Veneklaas EJ, Barrett-Lennard EG, Colmer TD.. 2017. Hydraulic redistribution: limitations for plants in saline soils. Plant, Cell & Environment 40: 2437–2446. doi:10.1111/pce.13020. PubMed DOI

Bechtold WA. 2003. Crown position and light exposure classification-an alternative to field-assigned crown class. Northern Journal of Applied Forest 20: 154–160.

Blaedow RA, Juzwik J.. 2010. Spatial and temporal distribution of Ceratocystis fagacearum in roots and root grafts of Oak wilt affected Red Oaks. Arboriculture & Urban Forestry 36: 28–34.

Bormann FH. 1966. The structure, function, and ecological significance of root grafts in Pinus strobus. Ecological Monographs 36: 1–26. doi:10.2307/1948486. DOI

Bormann FH, Graham BF.. 1959. The occurrence of natural root grafting in Eastern White Pine, Pinus Strobus L., and its ecological implications. Ecology 40: 677–691. doi:10.2307/1929820. DOI

Burgess SSO, Adams MA, Turner NC, Ong CK.. 1998. The redistribution of soil water by tree root systems. Oecologia 115: 306–311. doi:10.1007/s004420050521. PubMed DOI

De La Rue C. 1934. Root grafting in trees. American Journal of Botany 21: 121–126.

De Swaef T, De Schepper V, Vandegehuchte MW, Steppe K.. 2015. Stem diameter variations as a versatile research tool in ecophysiology. Tree Physiology 35: 1047–1061. doi:10.1093/treephys/tpv080. PubMed DOI

Dosen RC, Iyer JG.. 1979. Effect of grafted roots of stumps on the growth of a thinned red pine plantation. Tree Planters’ Notes 30: 19–21.

Eis S. 1972. Root grafts and their silvicultural implications. Canadian Journal of Forest Research 2: 111–120. doi:10.1139/x72-022. DOI

Fraser EC, Lieffers VJ, Landhäusser SM.. 2006. Carbohydrate transfer through root grafts to support shaded trees. Tree Physiology 26: 1019–1023. doi:10.1093/treephys/26.8.1019. PubMed DOI

Fraser EC, Lieffers VJ, Landhäusser SM.. 2007. The persistence and function of living roots on lodgepole pine snags and stumps grafted to living trees. Annals of Forest Science 64: 31–36. doi:10.1051/forest:2006085. DOI

Gaspard DT, DesRochers A.. 2020. Natural root grafting in hybrid poplar clones. Trees - Structure and Function 34: 881–890.

Gordon DE. 1974. The importance of root grafting in the spread of phytophthora root rot in an immature stand of Port-Orford-cedar. Portland: Oregon State University. https://ir.library.oregonstate.edu/concern/graduate_thesis_or_dissertations/3t945w349.

Graham BF, Bormann FH.. 1966. Natural root grafts. The Botanical Review 32: 255–292. doi:10.1007/bf02858662. DOI

Grimm V, Berger U.. 2016. Robustness analysis: deconstructing computational models for ecological theory and applications. Ecological Modelling 326: 162–167. doi:10.1016/j.ecolmodel.2015.07.018. DOI

Grimm V, Revilla E, Berger U, et al. . 2005. Pattern-oriented modeling of agent-based complex systems: lessons from ecology. Science 310: 987–991. doi:10.1126/science.1116681. PubMed DOI

Hao G-Y, Jones TJ, Luton C, et al. . 2009. Hydraulic redistribution in dwarf Rhizophora mangle trees driven by interstitial soil water salinity gradients: impacts on hydraulic architecture and gas exchange. Tree Physiology 29: 697–705. doi:10.1093/treephys/tpp005. PubMed DOI

Hedderich J, Sachs L.. 2020. Angewandte Statistik. Methodensammlung mit R. Berlin: Springer-Verlag.

Jelínková H, Tremblay F, Desrochers A.. 2012. Herbivore-simulated induction of defenses in clonal networks of trembling aspen (Populus tremuloides). Tree Physiology 32: 1348–1356. doi:10.1093/treephys/tps094. PubMed DOI

Jones TW, Bretz TW.. 1958. Experimental oak wilt control in Missouri. Research Bulletin 657.

Juzwik J, O’Brien J, Evenson C, Castillo P, Mahal G.. 2010. Controlling spread of the Oak wilt pathogen (Ceratocystis fagaceorum) in a Minnesota urban forest park reserve. Arboriculture and Urban Forestry 36: 171–178.

Külla T, Lõhmus K.. 1999. Influence of cultivation method on root grafting in Norway spruce (Picea abies (L.) Karst.). Plant and Soil 217: 91–100.

Lev-Yadun S. 2011. Why should trees have natural root grafts? Tree Physiology 31: 575–578. doi:10.1093/treephys/tpr061. PubMed DOI

Lin G, Sternberg LS.. 1992. Comparative study of water uptake and photosynthetic gas exchange between scrub and fringe red mangroves, Rhizophora mangle L. Oecologia 90: 399–403. PubMed

Melcher PJ, Goldstein G, Meinzer FC, et al. . 2001. Water relations of coastal and estuarine Rhizophora mangle: xylem pressure potential and dynamics of embolism formation. Oecologia 126: 182–192. doi:10.1007/s004420000519. PubMed DOI

Meyer D, Dimitriadou E, Hornik K, Weingessel A, Leisch F.. 2019. e1071: Misc Functions of the Department of Statistics, Probability Theory Group (Formerly: E1071), TU Wien. https://CRAN.R-project.org/package=e1071

Munns R, Tester M.. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651–681. doi:10.1146/annurev.arplant.59.032607.092911. PubMed DOI

Nakagawa S, Johnson PCD, Schielzeth H.. 2017. The coefficient of determination R2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. Journal of the Royal Society Interface 14: 20170213. doi:10.1098/rsif.2017.0213. PubMed DOI PMC

Oliveira RS, Christoffersen BO, de V. Barros F, et al. . 2014. Changing precipitation regimes and the water and carbon economies of trees. Theoretical and Experimental Plant Physiology 26: 65–82.

O’Neal ES, Davis DD.. 2015. Intraspecific root grafts and clonal growth within Ailanthus altissima stands influence Verticillium nonalfalfae transmission. Plant Disease 99: 1070–1077. doi:10.1094/PDIS-07-14-0722-RE. PubMed DOI

Passioura JB. 1988. Water transport in and to roots. Annual Review of Plant Physiology and Plant Molecular Biology 39: 245–265. doi:10.1146/annurev.pp.39.060188.001333. DOI

Peters R, Lovelock C, López-Portillo J, et al. . 2021. Partial canopy loss of mangrove trees: mitigating water scarcity by physical adaptation and feedback on porewater salinity. Estuarine, Coastal and Shelf Science 248: 106797. doi:10.1016/j.ecss.2020.106797. DOI

Peters R, Olagoke A, Berger U.. 2018. A new mechanistic theory of self-thinning: adaptive behaviour of plants explains the shape and slope of self-thinning trajectories. Ecological Modelling 390: 1–9. doi:10.1016/j.ecolmodel.2018.10.005. DOI

Peters R, Vovides AG, Luna S, Grüters U, Berger U.. 2014. Changes in allometric relations of mangrove trees due to resource availability – a new mechanistic modelling approach. Ecological Modelling 283: 53–61. doi:10.1016/j.ecolmodel.2014.04.001. DOI

Quer E, Baldy V, DesRochers A.. 2020. Forest ecology and management ecological drivers of root grafting in balsam fir natural stands. Forest Ecology and Management 475: 118388. doi:10.1016/j.foreco.2020.118388. DOI

R Core Team. 2020. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

Rao AN. 1966. Developmental anatomy of natural root grafts in Ficus Globosa. Australian Journal of Botany 14: 269–276.

Richards JH, Caldwell MM.. 1987. Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia (Berlin) 73: 486–489. PubMed

Rodriguez-Dominguez CM, Brodribb TJ.. 2020. Declining root water transport drives stomatal closure in olive under moderate water stress. New Phytologist 225: 126–134. PubMed

Salomón RL, Tarroux E, DesRochers A.. 2016. Natural root grafting in Picea mariana to cope with spruce budworm outbreaks. Canadian Journal of Forest Research 46: 1059–1066. doi:10.1139/cjfr-2016-0121. DOI

Schreel JDM, Van de Wal BAE, Hervé-Fernandez P, Boeckx P, Steppe K.. 2019. Hydraulic redistribution of foliar absorbed water causes turgor-driven growth in mangrove seedlings. Plant, Cell & Environment 42: 2437–2447. doi:10.1111/pce.13556. PubMed DOI

Schubert S. 2011. Pflanzenernährung: Grundwissen Bachelor. Stuttgart: Eugen Ulmer KG.

Schultz RP. 1963. Occurrence of stump callusing in second-growth Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco). Master's Thesis, Portland: Oregon State University. https://ir.library.oregonstate.edu/concern/graduate_thesis_or_dissertations/6d56zz98c.

Shepperd WD. 1993. Initial growth, development, and clonal dynamics of regenerated aspen in the Rocky Mountains. U.S. Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station; RM-312.

Shinozaki K, Yoda K, Hozumi K, Kira T.. 1964. A quantitative analysis of plant form - the pipe model theory II. Further evidence of the theory and its application in forest ecology. Japanese Journal of Ecology 14: 133–139.

Sobrado MA. 2001. Hydraulic properties of a mangrove Avicennia germinans as affected by NaCl. Biologia Plantarum 44: 435–438. doi:10.1023/a:1012479718305. DOI

Stone J, Stone E.. 1975. The communal root system of red pine: water conduction through root grafts. Forest Science 21: 255–261.

Suárez N, Sobrado MA.. 2000. Adjustments in leaf water relations of mangrove (Avicennia germinans) seedlings grown in a salinity gradient. Tree Physiology 20: 277–282. doi:10.1093/treephys/20.4.277. PubMed DOI

Tarroux E, DesRochers A.. 2011. Effect of natural root grafting on growth response of jack pine (Pinus banksiana; Pinaceae). American Journal of Botany 98: 967–974. doi:10.3732/ajb.1000261. PubMed DOI

Tarroux E, DesRochers A, Krause C.. 2010. Effect of natural root grafting on growth response of jack pine (Pinus banksiana) after commercial thinning. Forest Ecology and Management 260: 526–535. doi:10.1016/j.foreco.2010.05.008. DOI

Vovides AG, Marín-Castro B, Barradas G, Berger U, López-Portillo J.. 2016. A simple and cost-effective method for cable root detection and extension measurement in estuary wetland forests. Estuarine, Coastal and Shelf Science 183: 117–122. doi:10.1016/j.ecss.2016.10.029. DOI

Vovides AG, Vogt J, Kollert A, et al. . 2014. Morphological plasticity in mangrove trees: salinity-related changes in the allometry of Avicennia germinans. Trees 28: 1413–1425.

Vovides AG, Wimmler M-C, Schrewe F, et al. . 2021. Roots of cooperation: can root graft networks benefit trees under stress?. Communications Biology, in press. PubMed PMC

Warren JM, Brooks JR, Meinzer FC, Eberhart JL.. 2008. Hydraulic redistribution of water from Pinus ponderosa trees to seedlings: evidence for an ectomycorrhizal pathway. New Phytologist 178: 382–394. doi:10.1111/j.1469-8137.2008.02377.x. PubMed DOI

Wimmler M-C, Bathmann J, Peters R, et al. . 2021. Plant–soil feedbacks in mangrove ecosystems: establishing links between empirical and modelling studies. Trees 35: 1423–1438.

Wood JP. 1970. Root grafting in Pinus Radiata D.Don. Master’s thesis, Australian National University. https://openresearch-repository.anu.edu.au/handle/1885/143227.

Yli-Vakkuri P. 1953. Untersuchungen über Organische Wurzelverbindungenzwischen Bäumen in Kiefernbeständen. Acta Forestalia Fennica. Suomen metsätieteellinen seura (SMS) - The Finnish Society of Forest Science. http://hdl.handle.net/10138/17996

Yoder CK, Nowak RS.. 1999. Hydraulic lift among native plant species in the Mojave Desert. Plant and Soil 215: 93–102.

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