Excess vegetative growth and irregular fruit-bearing are often undesirable in horticultural practice. However, the biological mechanisms underlying these traits in fruit trees are not fully understood. Here, we tested if growth vigour and susceptibility of apple and pear trees to alternate fruit-bearing are associated with vascular anatomy. We examined anatomical traits related to water transport and nutrient storage in young woody shoots and roots of 15 different scion/rootstock cultivars of apple and pear trees. In addition, soil and leaf water potentials were measured across a drought period. We found a positive correlation between the mean vessel diameter of roots and the annual shoot length. Vigorously growing trees also maintained less negative midday leaf water potential during drought. Furthermore, we observed a close negative correlation between the proportions of total parenchyma in the shoots and the alternate bearing index. Based on anatomical proxies, our results suggest that xylem transport efficiency of rootstocks is linked to growth vigour of both apple and pear trees, while limited carbohydrate storage capacity of scions may be associated with increased susceptibility to alternate bearing. These findings can be useful for the breeding of new cultivars of commercially important fruit trees.

Department of Biology Faculty of Science University of Hradec Králové Hradec Králové Czech Republic

Research and Breeding Institute of Pomology Hořice Czech Republic

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Albacete A., Martínez-Andújar C., Merínez-Pérez A., Thompson A.J., Dodd I.C., Pérez-Alfocea F. (2015) Unravelling rootstock×scion interactions to improve food security. Journal of Experimental Botany, 66, 2211-2226.

Aloni R. (1987) Differentiation of vascular tissues. Annual Review of Plant Physiology, 38, 179-204.

An H., Luo F., Wu T., Wang Y., Xu X., Zhang X., Han Z. (2017) Dwarfing effect of apple rootstocks is intimately associated with low number of fine roots. HortScience, 52, 503-512.

Anfodillo T., Petit G., Crivellaro A. (2013) Axial conduit widening in woody species: a still neglected anatomical pattern. IAWA Journal, 34, 352-364.

Atkinson C.J., Else M.A., Taylor L., Dover C.J. (2003) Root and stem hydraulic conductivity as determinants of growth potential in grafted trees of apple (Malus pumila Mill.). Journal of Experimental Botany, 54, 1221-1229.

Atkinson C.J., Policarpo M., Webster A.D., Kuden A.M. (1999) Drought tolerance of apple rootstocks: Production and partitioning of dry matter. Plant and Soil, 206, 223-235.

Baninasab B., Rahemi M. (2006) Possible role of non-structural carbohydrates in alternate bearing of pistachio. European Journal of Horticultural Science, 71, 277-282.

Basile B., DeJong T.M. (2018) Control of fruit tree vigor induced by dwarfing rootstocks. In: Warrington I. (Ed), Horticultural Reviews. John Wiley & Sons, Hoboken, NY, USA, pp 39-97.

Basile B., Marsal J., DeJong T.M. (2003a) Daily shoot extension growth of peach trees growing on rootstocks that reduce scion growth to daily dynamics of stem water potential. Tree Physiology, 23, 695-704.

Basile B., Marsal J., Solari L.I., Tyree M.T., Bryla D.R., DeJong T.M. (2003b) Hydraulic conductance of peach trees grafted on rootstocks with differing size-controlling potentials. The Journal of Horticultural Science and Biotechnology, 78, 768-774.

Bauerle T.L., Centinari M., Bauerle W.L. (2011) Shifts in xylem vessel diameter and embolisms in grafted apple trees of differing rootstock growth potential in response to drought. Planta, 234, 1045-1054.

Beakbane A.B. (1952) Anatomical structure in relation to rootstock behaviour. In: Synge P.M. (Ed.), Proceedings 13th International Horticultural Congress, vol. 1. London, UK. pp. 152-157.

Beakbane A.B., Thompson E.C. (1940) Anatomical studies of stems and roots of hardy fruit trees II. The internal structure of the roots of some vigorous and some dwarfing apple rootstocks, and the correlation of structure with vigour. Journal of Pomology and Horticultural Science, 17, 141-149.

Berman M.E., DeJong T.M. (1997) Diurnal patterns of stem extension growth in peach (Prunus persica): temperature and fluctuations in water status determine growth rate. Physiologia Plantarum, 100, 361-370.

Bruckner C.H., DeJong T.M. (2014) Proposed pre-selection method for identification of dwarfing peach rootstocks based on rapid shoot xylem vessel analysis. Scientia Horiculturae, 165, 404-409.

Capelli M., Lauri P.É., Normand F. (2016) Deciphering the costs of reproduction in mango - vegetative growth matters. Frontiers in Plant Science, 7, 1531.

Chen B., Wang C., Tian Y., Chu Q., Hu C. (2015) Anatomical characteristics of young stems and mature leaves of dwarf pear. Scientia Horiculturae, 186, 172-179.

Chen Z., Zhu S., Zhang Y., Luan J., Li S., Sun P., Wan X., Liu S. (2020) Tradeoff between storage capacity and embolism resistance in the xylem of temperate broadleaf tree species. Tree Physiology, 40, 1029-1042.

Comas L.H., Bouma T.J., Eissenstat D.M. (2002) Linking root traits to potential growth rate in six temperate tree species. Oecologia, 132, 34-43.

Comstock J., Mencuccini M. (1998) Control of stomatal conductance by leaf water potential in Hymenoclea salsola (T. & G.), a desert subshrub. Plant, Cell & Environment, 21, 1029-1038.

Cruiziat P., Cochard H., Améglio T. (2002) Hydraulic architecture of trees: main concepts and results. Annals of Forest Science, 59, 723-752.

De Silva H.N., Hall A.J., Tustin D.S., Gandar P.W. (1999) Distribution of root length density of apple trees on different dwarfing rootstocks. Annals of Botany, 83, 335-345.

Doblas V.G., Geldner N., Barberon M. (2017) The endodermis, a tightly controlled barrier for nutrients. Current Opinion in Plant Biology, 39, 136-143.

FAO. (2019) FAO Statistics Data 2019. Available at http://www.fao.org/faostat/en/#data (accessed 21 May 2020).

Fazio G., Wan Y., Kviklys D., Romero L., Adams R., Strickland D., Robinson T. (2014) Dw2, a new dwarfing locus in apple rootstocks and its relationship to induction of early bearing in apple scions. Journal of the American Society for Horticultural Science, 139, 87-98.

Fichot R., Chamaillard S., Depardieu C., Le Thiec D., Cochard H., Barigah T.S., Brignolas F. (2011) Hydraulic efficiency and coordination with xylem resistance to cavitation, leaf function, and growth performance among eight unrelated Populus deltoides × Populus nigra hybrids. Journal of Experimental Botany, 62, 2093-2106.

Fichot R., Laurans F., Monclus R., Moreau A., Pilate G., Brignolas F. (2009) Xylem anatomy correlates with gas exchange, water-use efficiency and growth performance under contrasting water regimes: evidence from Populus deltoides × Populus nigra hybrids. Tree Physiology, 29, 1537-1549.

Foster T.M., McAtee P.A., Waite C.N., Boldingh H.L., McGhie T.K. (2017) Apple dwarfing rootstocks exhibit an imbalance in carbohydrate allocation and reduced cell growth and metabolism. Horticulture Research, 4, 17009.

Gleason S.M., Butler D.W., Ziemińska K., Waryszak P., Westoby M. (2012) Stem xylem conductivity is key to plant water balance across Australian angiosperm species. Functional Ecology, 26, 343-352.

Goldschmidt E.E. (2005) Regolazione dell’alternanza di produzione negli alberi da fruto (Italia). Italus Hortus, 12, 11-17.

Goldschmidt E.E. (2013) The evolution of fruit tree productivity: a review. Economic Botany, 67, 51-62.

Goncalves B., Correia C.M., Silva A.P., Bacelar E.A., Santos A., Ferreira H., Moutinho-Pereira J.M. (2007) Variation in xylem structure and function in roots and stems of scion-rootstock combinations of sweet cherry tree (Prunus avium L.). Trees, 21, 121-130.

Goncalves B., Moutinho-Pereira J., Santos A., Silva A.P., Bacelar E., Correia C., Rosa E. (2005) Scion-rootstock interaction affects the physiology and fruit quality of sweet cherry. Tree Physiology, 26, 93-104.

Guerriero G., Hausman J.-F., Cai G. (2014) No stress! Relax! Mechanisms governing growth and shape in plant cells. International Journal of Molecular Sciences, 15, 5094-5114.

Hajagos A., Végvári G. (2013) Investigation of tissue structure and xylem anatomy of eight rootstocks of sweet cherry (Prunus avium L.). Trees, 27, 53-60.

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

Hoblyn T., Grubb N., Painter A., Wates B. (1936) Studies in biennial bearing - I. Journal of Pomology and Horticultural Science, 14, 39-76.

Jackson J.E. (2003) Biology of horticultural crops: Biology of apples and pears. Cambridge University Press, Edinburgh, UK, pp 500.

Jones O.P. (1976) Effect of dwarfing interstocks on the xylem sap composition in apple trees. Effect on nitrogen, potassium, phosphorus, calcium and magnesium content. Annals of Botany, 40, 1231-1235.

Jupa R., Plavcová L., Gloser V., Jansen S. (2016) Linking xylem water storage with anatomical parameters in five temperate tree species. Tree Physiology, 36, 756-769.

Kiorapostolou N., Da Sois L., Petruzzellis F., Savi T., Trifilò P., Nardini A., Petit G. (2019) Vulnerability to xylem embolism correlates to wood parenchyma fraction in angiosperms but not in gymnosperms. Tree Physiology, 39, 1675-1684.

Laur J., Hacke U.G. (2013) Transpirational demand affects aquaporin expression in poplar roots. Journal of Experimental Botany, 64, 2283-2293.

Lauri P.E., Combe F., Brun L. (2014) Regular bearing in the apple - Architectural basis for an early diagnosis on the young tree. Scientia Horiculturae, 174, 10-16.

Lauri P.E., Térouanne E., Lespinasse J.M., Regnard J.L., Kelner J.J. (1995) Genotypic differences in the axillary bud growth and fruiting pattern of apple fruit branches over several years - an approach to regulation of fruit bearing. Scientia Horiculturae, 64, 265-281.

Lechthaler S., Turnbull T.L., Gelmini Y., Pirotti F., Anfodillo T., Adams M.A., Petit G. (2019) A standardization method to disentangle environmental information from axial trends of xylem anatomical traits. Tree Physiology, 39, 495-502.

Ma L., Hou C.W., Zhang X.Z., Li H.L., Han D.G., Wang Y., Han Z.H. (2013) Seasonal growth and spatial distribution of apple tree roots on different rootstocks or interstems. Journal of the American Society for Horticultural Science, 138, 79-87.

Martínez-Alcántara B., Iglesias D.J., Reig C., Mesejo C., Agustí M., Primo-Millo E. (2015) Carbon utilization by fruit limits shoot growth in alternate-bearing citrus trees. Journal of Plant Physiology, 15, 108-117.

Martínez-Alcántara B., Rodriguez-Gamir J., Martínez-Cuenca M.R., Iglesias D.J., Primo-Millo E., Forner-Giner M.A. (2013) Relationship between hydraulic conductance and citrus dwarfing by the Flying Dragon rootstock (Poncirus trifoliata L. Raft var. monstruosa). Trees, 27, 629-638.

Mészáros M., Kosina J., Laňar L., Náměstek J. (2015) Long-term evaluation of growth and yield of Stanley and Cacanska lepotica plum cultivars on selected rootstocks. Horticultural Science, 42, 22-28.

Mészáros M., Laňar L., Kosina J., Náměstek J. (2019) Aspects influencing the rootstock - scion performance during long term evaluation in pear orchard. Horticultural Science, 46, 1-8.

Monselise S.P., Goldschmidt E.E. (1982) Alternate bearing in fruit trees: a review. Horticultural Reviews, 4, 128-173.

Morris H., Gillingham M.A., Plavcová L., Gleason S.M., Olson M.E., Coomes D.A., Fichtler E., Klepsch M.M., Martínez-Cabrera H.I., McGlinn D.J., Wheeler E.A., Zheng J., Zieminska K., Jansen S. (2018) Vessel diameter is related to amount and spatial arrangement of axial parenchyma in woody angiosperms. Plant, Cell & Environment, 41, 245-260.

Muleo R., Intrieri M.C., Iacona C., Maggi E., Loreti F. (2011) Peach rootstocks inducing different vigour reflect genomic, physiological and morphological diversity in roots. Acta Horticulturae, 903, 113-120.

Nardini A., Gasco A., Raimondo F., Gortan E., Lo Gullo M.A., Caruso T., Salleo S. (2006) Is rootstock-induced dwarfing in olive an effect of reduced plant hydraulic efficiency? Tree Physiology, 26, 1137-1144.

Olien W.C., Lakso A.N. (1986) Effect of rootstock on apple (Malus domestica) tree water relations. Physiologia Plantarum, 67, 421-430.

Olmstead M.A., Lang N.S., Ewers F., Owens S. (2006) Xylem vessel anatomy of sweet cherries (Prunus avium L.) grafted onto dwarfing and non-dwarfing rootstocks. Journal of the American Society for Horticultural Science, 131, 577-585.

Olson M.E., Anfodillo T., Rosell J.A., Petit G., Crivellaro A., Isnard S., León-Gómez C., Alvarado-Cárdenas L.O., Castorena M. (2014) Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates. Ecology Letters, 19, 240-248.

Pfautsch S., Harbusch M., Wesolowski A., Smith R., Macfarlane C., Tjoelker M.G., Reich P.B., Adams M.A. (2016) Climate determines vascular traits in the ecologically diverse genus Eucalyptus. Ecology Letters, 19, 240-248.

Pfautsch S., Renard J., Tjoelker M., Salih A. (2015) Phloem as capacitor - radial transfer of water into xylem of tree stems seems to occur via symplastic transport in ray parenchyma. Plant Physiology, 167, 963-971.

Plavcová L., Morris H., Hoch G., Ghiasi S., Jansen S. (2016) The amount of parenchyma and living fibres affects storage of non-structural carbohydrates in young stems and roots of temperate trees. American Journal of Botany, 103, 603-612.

Pratt R.B., Jacobsen A.L. (2017) Conflicting demands on angiosperm xylem: Tradeoffs among storage, transport and biomechanics. Plant, Cell & Environment, 40, 897-913.

R Development Core Team (2010) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/

Reighard G.L., Loreti F. (2008) Rootstock development. In: Layne D. R., Bassi D. (Eds), The peach: Botany, production and uses. CABI, Wallingford, UK, pp 193-220.

Rodriguez-Dominguez C.M., Buckley T.N., Egea G., de Cires A., Hernandez-Santana V., Martorell S., Diaz-Espejo A. (2016) Most stomatal closure in woody species under moderate drought can be explained by stomatal responses to leaf turgor. Plant, Cell & Environment, 39, 2014-2026.

Rosell J.A. (2019) Bark in woody plants: understanding the diversity of a multifunctional structure. Integrative and Comparative Biology, 59, 535-547.

Sacks M.M., Silk W.K., Burman P. (1997) Effect of water stress on cortical cell division rates within the apical meristem of primary roots of maize. Plant Physiology, 114, 519-527.

Sauter J.J., van Cleve B. (1992) Seasonal variation of amino acids in the xylem sap of “Populus × canadensis” and its relation to protein body mobilization. Trees, 7, 26-32.

Słupianek A., Kasprowicz-Maluśki A., Myśkow E., Turzańska M., Sokołowska K. (2019) Endocytosis acts as transport pathway in wood. New Phytologist, 222, 1846-1861.

Sokolowska K., Zagórska-Marek B. (2012) Symplasmic, long-distance transport in xylem and cambial regions in branches of Acer pseudoplatanus (Aceraceae) and Populus tremula × P. tremuloides (Salicaceae). American Journal of Botany, 99, 1745-1755.

Solari L.I., Johnson S., DeJong T.M. (2006a) Relationship of water status to vegetative growth and leaf gas exchange of peach (Prunus persica) trees on different rootstocks. Tree Physiology, 26, 1333-1341.

Solari L.I., Pernice F., DeJong T.M. (2006b) The relationship of hydraulic conductance to root system characteristics of peach (Prunus persica) rootstocks. Physiologia Plantarum, 128, 324-333.

Somelidou K., Morris D.A., Battey N.H., Barnett J.R., John P. (1994) Auxin transport capacity in relation to the dwarfing effect of apple rootstocks. Journal of Horticultural Science, 69, 719-725.

Sperry J.S. (2000) Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology, 104, 13-23.

Tombesi S., Almehdi A., DeJong T.M. (2011) Phenotyping vigour control capacity of new peach rootstocks by xylem vessel analysis. Scientia Horiculturae, 127, 353-357.

Tombesi S., Johnson R.S., Day K.R., DeJong T.M. (2010a) Relationships between xylem vessel characteristics, calculated axial hydraulic conductance and size controlling capacity of peach rootstocks. Annals of Botany, 105, 327-331.

Tombesi S., Johnson R.S., Day K.R., DeJong T.M. (2010b) Interactions between rootstock, inter-stem and scion xylem vessel characteristics of peach trees growing on rootstocks with contrasting size-controlling characteristics. AoB Plants, 10, plq013.

Trifilo P., Lo Gullo M.A., Nardini A., Pernice F., Salleo S. (2007) Rootstock effects on xylem conduit dimensions and vulnerability to cavitation of Olea europaea L. Trees, 21, 549-556.

Tyree M.T., Sperry J.S. (1988) Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Plant Physiology, 88, 574-580.

Tyree M.T., Velez V., Dalling J.W. (1998) Growth dynamics of root and shoot hydraulic conductance in seedlings of five neotropical tree species: scaling to show possible adaptation to differing light regimes. Oecologia, 114, 293-298.

Tyree M.T., Zimmermann M.H. (2002) Xylem structure and ascent of sap. Springer, Berlin, Germany, pp. 331.

Webster A.D. (2004) Vigour mechanisms in dwarfing rootstocks for temperate fruit trees. Acta Horticulturae, 658, 29-41.

Weibel A., Johnson R.S., DeJong T.M. (2003) Comparative vegetative growth responses of two peach cultivars grown on size-controlling versus standard rootstocks. Journal of the American Society for Horticultural Science, 128, 463-471.

Ziemińska K., Wright I.J., Westoby M. (2015) Broad anatomical variation within a narrow wood density range - a study of twig wood across 69 Australian angiosperms. PLoS One, 10, e0124892.

Relationships between trunk radial growth and fruit yield in apple and pear trees on size-controlling rootstocks