Phenotyping xylem connections in grafted plants using X-ray micro-computed tomography.

3D imaging grafting grapevine micro‐CT scion stock

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
22 Mar 2024
Historique:
revised: 15 02 2024
received: 14 12 2023
accepted: 03 03 2024
medline: 22 3 2024
pubmed: 22 3 2024
entrez: 22 3 2024
Statut: aheadofprint

Résumé

Plants are able to naturally graft or inosculate their trunks, branches and roots together, this mechanism is used by humans to graft together different genotypes for a range of purposes. Grafts are considered successful if functional vascular connections between the two genotypes occur. Various techniques can evaluate xylem connections across the graft interface. However, these methods are generally unable to assess the heterogeneity and three-dimensional (3D) structure of xylem vessel connections. Here we present the use of X-ray micro-computed tomography to characterize the 3D morphology of grafts of grapevine. We show that xylem vessels form between the two plants of natural root and human-made stem grafts. The main novelty of this methodology is that we were able to visualize the 3D network of functional xylem vessels connecting the scion and rootstock in human-made stem grafts thanks to the addition of a contrast agent to the roots and improved image analysis pipelines. In addition, we reveal the presence of extensive diagonal xylem connections between the main axial xylem vessels in 2-year old grapevine stems. In conclusion, we present a method that has the potential to provide new insights into the structure and function of xylem vessels in large tissue samples.

Identifiants

pubmed: 38516728
doi: 10.1111/pce.14883
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Interreg
Organisme : Association Instituts Carnot
Organisme : Agence Nationale de la Recherche
Organisme : GPR Bordeaux Plant Sciences

Informations de copyright

© 2024 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.

Références

Bahar, E., Korkutal, I., Carbonneau, A. & Akcay, G. (2010) Using magnetic resonance imaging technique (MRI) to investigate graft connection and its relation to reddening discoloration in grape leaves. Journal of Food, Agriculture & Environment, 8, 293–297.
Bormann, F.H. (1966) The structure, function, and ecological significance of root grafts in Pinus strobus L. Ecological Monographs, 36, 1–26.
Brodersen, C.R. (2013) Visualizing wood anatomy in three dimensions with high‐resolution x‐ray micro‐tomography (μCT) – a review. IAWA Journal, 34, 408–424.
Brodersen, C.R., Choat, B., Chatelet, D.S., Shackel, K.A., Matthews, M.A. & McElrone, A.J. (2013) Xylem vessel relays contribute to radial connectivity in grapevine stems (Vitis vinifera and V. arizonica; Vitaceae). American Journal of Botany, 100, 314–321.
Brodersen, C.R., Lee, E.F., Choat, B., Jansen, S., Phillips, R.J. & Shackel, K.A. et al. (2011) Automated analysis of three‐dimensional xylem networks using high‐resolution computed tomography. New Phytologist, 191, 1168–1179.
Carrere, C., Spilmont, A.S., Loupit, G., Beutin, P., Stessels, C., Ollat, N. et al. (2022) Evaluation of criteria to assist the selection of good quality grafted grapevines prior to their commercialisation. OENO One, 56, 15–27.
Chatelet, D.S., Matthews, M.A. & Rost, T.L. (2006) Xylem structure and connectivity in grapevine (Vitis vinifera) shoots provides a passive mechanism for the spread of bacteria in grape plants. Annals of Botany, 98, 483–494.
Cochard, H., Delzon, S. & Badel, E. (2015) X‐ray microtomography (micro‐CT): a reference technology for high‐resolution quantification of xylem embolism in trees. Plant, Cell & Environment, 38, 201–206.
Espen, L., Cocucci, M. & Sacchi, G.A. (2005) Differentiation and functional connection of vascular elements in compatible and incompatible pear/quince internode micrografts. Tree Physiology, 25, 1419–1425.
Fernandez, R. & Moisy, C. (2020) Fijiyama: a registration tool for 3D multimodal time‐lapse imaging. Bioinformatics, 37, 1482–1484.
Frank, M.H., Komarov, S., Wang, Q., Li, K., Hecking, M. & Fowler, H. et al. (2022) Integrated PET and confocal imaging informs a functional timeline for the dynamic process of vascular reconnection during grafting. bioRxiv, 2022.2010.2027.513862. [Preprint].
Fraser, E.C., Lieffers, V.J. & Landhäusser, S.M. (2005) Age, stand density, and tree size as factors in root and basal grafting of lodgepole pine. Canadian Journal of Botany, 83, 983–988.
Gärtner, H., Lucchinetti, S. & Schweingruber, F.H. (2014) New perspectives for wood anatomical analysis in dendrosciences: the GSL1‐microtome. Dendrochronologia, 32, 47–51.
Gaspard, D.T. & DesRochers, A. (2020) Natural root grafting in hybrid poplar clones. Trees, 34, 881–890.
Jahnke, S., Menzel, M.I., Van Dusschoten, D., Roeb, G.W., Bühler, J., Minwuyelet, S. et al. (2009) Combined MRI–PET dissects dynamic changes in plant structures and functions. The Plant Journal, 59, 634–644.
Kim, H.K. & Lee, S.J. (2010) Synchrotron X‐ray imaging for nondestructive monitoring of sap flow dynamics through xylem vessel elements in rice leaves. New Phytologist, 188, 1085–1098.
Korkutal, I., Bahar, E. & Ozdemir, A.G. (2018) Determining the internal connection ratios by MRI and their effects on grafted rooted vine growing features of cvs. Merlot and Syrah. Erwerbs‐Obstbau, 60, 61–69.
Lee, E., Matthews, M., McElrone, A., Phillips, R., Shackel, K. & Brodersen, C. (2013) Analysis of HRCT‐derived xylem network reveals reverse flow in some vessels. Journal of Theoretical Biology, 333, 146–155.
Lev‐Yadun, S. (2011) Why should trees have natural root grafts? Tree Physiology, 31, 575–578.
Loupit, G., Brocard, L., Ollat, N. & Cookson, S.J. (2023) Grafting in plants: recent discoveries and new applications. Journal of Experimental Botany, 74, 2433–2447.
Loupit, G. & Cookson, S.J. (2020) Identifying molecular markers of successful graft union formation and compatibility. Frontiers in Plant Science, 11, 610352.
McElrone, A.J., Manuck, C.M., Brodersen, C.R., Patakas, A., Pearsall, K.R. & Williams, L.E. (2021) Functional hydraulic sectoring in grapevines as evidenced by sap flow, dye infusion, leaf removal and micro‐computed tomography. AoB Plants, 13, 13.
Melnyk, C.W., Schuster, C., Leyser, O. & Meyerowitz, E.M. (2015) A developmental framework for graft formation and vascular reconnection in Arabidopsis thaliana. Current Biology, 25, 1306–1318.
Milien, M., Renault‐Spilmont, A.S., Cookson, S.J., Sarrazin, A. & Verdeil, J.L. (2012) Visualization of the 3D structure of the graft union of grapevine using X‐ray tomography. Scientia Horticulturae, 144, 130–140.
Mudge, K., Janick, J., Scofield, S. & Goldschmidt, E.E. (2009) A history of grafting. Horticultural Reviews, 35, 437–493.
Nolf, M., Lopez, R., Peters, J.M.R., Flavel, R.J., Koloadin, L.S., Young, I.M. et al. (2017) Visualization of xylem embolism by X‐ray microtomography: a direct test against hydraulic measurements. New Phytologist, 214, 890–898.
Pouget, R. 2015. Le Phylloxéra et les maladies de la Vigne. La lutte victorieuse des savants et des vignerons français, 1850‐1900. Paris, France: Edilivre‐Aparis.
Pouzoulet, J., Scudiero, E., Schiavon, M., Santiago, L.S. & Rolshausen, P.E. (2019) Modeling of xylem vessel occlusion in grapevine. Tree Physiology, 39, 1438–1445.
Pratt, R.B., Castro, V., Fickle, J.C., Madsen, A. & Jacobsen, A.L. (2020) Factors controlling drought resistance in grapevine (Vitis vinifera, chardonnay): application of a new microCT method to assess functional embolism resistance. American Journal of Botany, 107, 618–627.
Pratt, R.B. & Jacobsen, A.L. (2018) Identifying which conduits are moving water in woody plants: a new HRCT‐based method. Tree Physiology, 38, 1200–1212.
Schindelin, J., Arganda‐Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T. et al. (2012) Fiji: an open‐source platform for biological‐image analysis. Nature Methods, 9, 676–682.
Schöning, U. & Kollmann, R. (1997) Phloem translocation in regenerating in vitro heterografts of different compatibility. Journal of Experimental Botany, 48, 289–295.
Schreel, J.D.M., Brodersen, C., De Schryver, T., Dierick, M., Rubinstein, A. & Dewettinck, K. et al. (2022) Foliar water uptake does not contribute to embolism repair in beech (Fagus sylvatica L.). Annals of Botany, 129, 555–566.
Steppe, K., Cnudde, V., Girard, C., Lemeur, R., Cnudde, J.‐P. & Jacobs, P. (2004) Use of X‐ray computed microtomography for non‐invasive determination of wood anatomical characteristics. Journal of Structural Biology, 148, 11–21.
Tandonnet, J.P., Marguerit, E., Cookson, S.J. & Ollat, N. (2018) Genetic architecture of aerial and root traits in field‐grown grafted grapevines is largely independent. Theoretical and Applied Genetics, 131, 903–915.
Tarroux, E. & DesRochers, A. (2010) Frequency of root grafting in naturally and artificially regenerated stands of Pinus banksiana: influence of site characteristics. Canadian Journal of Forest Research, 40, 861–871.
Walker, N.C., White, S.M., McKay Fletcher, D., Ruiz, S.A., Rankin, K.E., De Stradis, A. et al. (2023) The impact of xylem geometry on olive cultivar resistance to Xylella fastidiosa: an image‐based study. Plant Pathology, 72, 521–535.

Auteurs

Marilou Camboué (M)

EGFV, Univ. Bordeaux, Bordeaux Sciences Agro, INRAE, ISVV, Villenave d'Ornon, Bordeaux, France.

Anne Janoueix (A)

EGFV, Univ. Bordeaux, Bordeaux Sciences Agro, INRAE, ISVV, Villenave d'Ornon, Bordeaux, France.

Jean-Pascal Tandonnet (JP)

EGFV, Univ. Bordeaux, Bordeaux Sciences Agro, INRAE, ISVV, Villenave d'Ornon, Bordeaux, France.

Anne-Sophie Spilmont (AS)

IFV, French Institute of Vine and Wine, Domaine de l'Espiguette, Le Grau-du-Roi, France.

Cédric Moisy (C)

IFV, French Institute of Vine and Wine, Domaine de l'Espiguette, Le Grau-du-Roi, France.
UMR AGAP Institut, UMT Geno Vigne, CIRAD, INRAE, Institut Agro, Montpellier, France.

Guillaume Mathieu (G)

IFV, French Institute of Vine and Wine, Domaine de l'Espiguette, Le Grau-du-Roi, France.

Fabrice Cordelières (F)

Univ. Bordeaux, CNRS, INSERM, BIC, US4, UAR 3420, Bordeaux, France.

Jérémie Teillon (J)

Univ. Bordeaux, CNRS, INSERM, BIC, US4, UAR 3420, Bordeaux, France.

Luis Gonzaga Santesteban (LG)

Departement of Agronomy, Biotechnology and Food Science, Univ. Pública de Navarra UPNA, Pamplona, Navarra, Spain.

Nathalie Ollat (N)

EGFV, Univ. Bordeaux, Bordeaux Sciences Agro, INRAE, ISVV, Villenave d'Ornon, Bordeaux, France.

Sarah Jane Cookson (SJ)

EGFV, Univ. Bordeaux, Bordeaux Sciences Agro, INRAE, ISVV, Villenave d'Ornon, Bordeaux, France.

Classifications MeSH