Heterorhizy and fine root architecture of rabbiteye blueberry (Vaccinium virgatum) softwood-cuttings

Baba, Takashi; Nakaba, Satoshi; Noma, Satoshi; Funada, Ryo; Ban, Takuya

doi:10.1007/s10265-017-1000-y

Regular Paper
Published: 22 December 2017

Heterorhizy and fine root architecture of rabbiteye blueberry (Vaccinium virgatum) softwood-cuttings

Takashi Baba¹,
Satoshi Nakaba²,
Satoshi Noma³,
Ryo Funada² &
Takuya Ban³

Journal of Plant Research volume 131, pages 271–284 (2018)Cite this article

771 Accesses
6 Citations
1 Altmetric
Metrics details

Abstract

All fine root systems consist of individual fine roots. Individual roots have morphological, anatomical, and functional heterogeneity (heterorhizy). Heterorhizy plays crucial roles in plant ecosystems. However, in many species, the heterorhizy and fine root system architecture based on individual root units are unclear. This study investigated heterorhizy along the root system architecture of Vaccinium virgatum Ait (rabbiteye blueberry) softwood-cuttings (propagated from annual shoots in growing season) using protoxylem groups (PGs), a classification according to the number of protoxylem poles, as an indicator of individual root traits. Individual roots of rabbiteye blueberry varied from monarch to heptarch. The frequency of roots with larger number of PGs decreased but those with smaller number of PGs increased from adventitious roots toward lateral roots with different branching levels. This architecture were stable among cultivars, collecting position of the cuttings, or indole acetic acids treatment. Individual root sizes and secondary growth were positively correlated with the PGs. These results indicate that branching itself strongly and broadly controls individual root traits. The individual roots were classified into two types: monarch and diarch roots with small size and lacking secondary growth (thought to be hair roots in core Ericaceae) and triarch or more PG roots with large size and showing secondary growth. These heterogeneous individual roots responded differently to the experimental factors. In particular, elongation of the large roots significantly contributed to increased total root length. These results mean that heterorhizic plasticity is a determinant of root system development and heterorhizic variation exists even under practical cutting condition. In conclusion, we demonstrated heterorhizy of rabbieye blueberry cuttings based on the strong relationships of PG, individual root morphology and growth potential, and root system architecture. This study also supports strong connection between root morphology and functional roles intermediated by the PG.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

References

Allaway WG, Ashford AE (1996) Structure of hair roots in Lysinema ciliatum R. Br. and its implications for their water relations. Ann Bot 77:383–388. https://doi.org/10.1006/anbo.1996.0046
Article Google Scholar
Ashford AE, Allaway WG, Reed ML (1996) A possible role for the thick-walled epidermal cells in the mycorrhizal hair roots of Lysinema ciliatum R. Br. and other Epacridaceae. Ann Bot 77:375–381. https://doi.org/10.1006/anbo.1996.0045
Article Google Scholar
Bagniewska-Zadworna A, Byczyk J, Eissenstat DM et al (2012) Avoiding transport bottlenecks in an expanding root system: Xylem vessel development in fibrous and pioneer roots under field conditions. Am J Bot 99:1417–1426. https://doi.org/10.3732/ajb.1100552
Article PubMed Google Scholar
Ban T, Kushizaki K, Adachi F et al (2013) Development of rooting media including rice husk for blueberry cuttings. Hort Res (Japan) 12:131–134. https://doi.org/10.2503/hrj.12.131
Article Google Scholar
Beijerinck W (1940) Calluna: a monograph on the scotch heather. Verh K Akad Wet 38:1–80
Google Scholar
Biggs RH, Webb PG, Kossuth SV (1983) Rooting characteristics of eight rabbiteye blueberries recommended for Florida. Proc Florida State Hortic Soc 96:228–229
Google Scholar
Bonacorsi NK, Seago JL (2016) Root development and structure in seedlings of Ginkgo biloba. Am J Bot 103:355–363. https://doi.org/10.3732/ajb.1500312
CAS Article PubMed Google Scholar
Briggs CL, Ashfold AE (2001) Structure and composition of the thick wall in hair root epidermal cells of Woollsia pungens. New Phytol 149:219–232. https://doi.org/10.1046/j.1469-8137.2001.00031.x
Article Google Scholar
Brundrett MC, Enstone DE, Peterson CA (1988) A berberine-aniline blue fluorescent staining procedure for suberin, lignin, and callose in plant tissue. Protoplasma 146:133–142. https://doi.org/10.1007/BF01405922
Article Google Scholar
Brunner I, Herzog C, Dawes MA et al (2015) How tree roots respond to drought. Front Plant Sci 6:1–16. https://doi.org/10.3389/fpls.2015.00547
Article Google Scholar
Carlquist S, Schneider EL (2009) Do tracheid microstructure and the presence of minute crystals link Nymphaeaceae, Cabombaceae and Hydatellaceae? Bot J Linn Soc 159:572–582. https://doi.org/10.1111/j.1095-8339.2009.00960.x
Article Google Scholar
Celik H, Odabas MS (2009) Mathematical modeling of the indole-3-butyric acid applications on rooting of northern highbush blueberry (Vaccinium corymbosum L.) softwood-cuttings. Acta Physiol Plant 31:295–299. https://doi.org/10.1007/s11738-008-0232-9
CAS Article Google Scholar
Comas LH, Bouma TJ, Eissenstat DM (2002) Linking root traits to potential growth rate in six temperate tree species. Oecologia 132:34–43. https://doi.org/10.1007/s00442-002-0922-8
CAS Article PubMed Google Scholar
Dalpé Y (1986) Axenic synthesis of ericoid mycorrhiza in Vaccinium Angustifolium Ait. By Oidiodendron species. New Phytol 103:391–396. https://doi.org/10.1111/j.1469-8137.1986.tb00624.x
Article Google Scholar
Doi R, Tanikawa T, Miyatani K, Hirano Y (2017) Intraspecific variation in morphological traits of root branch orders in Chamaecyparis obtusa. Plant Soil. https://doi.org/10.1007/s11104-017-3230-0
Google Scholar
Eck P (1966) Botany. In: Eck P, Childers NF (eds) Blueberry culture. Rutgers University Press, New Jersey, pp 14–44
Google Scholar
Eissenstat DM, Achor DS (1999) Anatomical characteristics of roots of citrus rootstocks that vary in specific root length. New Phytol 141:309–321. https://doi.org/10.1046/j.1469-8137.1999.00342.x
Article Google Scholar
Emmett B, Nelson EB, Kessler A, Bauerle TL (2014) Fine-root system development and susceptibility to pathogen colonization. Planta 239:325–340. https://doi.org/10.1007/s00425-013-1989-7
CAS Article PubMed Google Scholar
Esau K (1965) Plant anatomy, 2nd edn. Wiley, New York
Google Scholar
Fitter A (1982) Morphometric analysis of root systems: application of the technique and influence of soil fertility on root system development in two herbaceous species. Plant Cell Environ 5:313–322. https://doi.org/10.1111/1365-3040.ep11573079
Google Scholar
Freudenstein JV, Broe MB, Feldenkris ER (2016) Phylogenetic relationships at the base of ericaceae: Implications for vegetative and mycorrhizal evolution. Taxon 65:794–804. https://doi.org/10.12705/654.7
Article Google Scholar
Gu J, Xu Y, Dong X et al (2014) Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species. Tree Physiol 34:415–425. https://doi.org/10.1093/treephys/tpu019
Article PubMed Google Scholar
Guo D, Xia M, Wei X et al (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683. https://doi.org/10.1111/j.1469-8137.2008.02573.x
Article PubMed Google Scholar
Hee J, Soh WY (1993) Vascular anatomy of the subterranean organ of Ophioglossum vulgatum L.. Plant Morphol 5:69–81. https://doi.org/10.5685/plmorphol.5.69
Article Google Scholar
Hishi T (2007) Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions. J For Res 12:126–133. https://doi.org/10.1007/s10310-006-0260-5
Article Google Scholar
Hishi T, Takeda H (2005a) Life cycles of individual roots in fine root system of Chamaecyparis obtusa Sieb. et Zucc. J For Res 10:181–187. https://doi.org/10.1007/s10310-004-0120-0
Article Google Scholar
Hishi T, Takeda H (2005b) Dynamics of heterorhizic root systems: Protoxylem groups within the fine-root system of Chamaecyparis obtusa. New Phytol 167:509–521. https://doi.org/10.1111/j.1469-8137.2005.01418.x
Article PubMed Google Scholar
Hodge A, Berta G, Doussan C et al (2009) Plant root growth, architecture and function. Plant Soil 321:153–187. https://doi.org/10.1007/s11104-009-9929-9
CAS Article Google Scholar
Horsley SB, Wilson BF (1971) Development of the woody portion of the root system of Betula papyrifera. Am J Bot 58:141–147
Article Google Scholar
Karahara I, Ikeda A, Kondo T, Uetake Y (2004) Development of the Casparian strip in primary roots of maize under salt stress. Planta 219:41–47. https://doi.org/10.1007/s00425-004-1208-7
CAS Article PubMed Google Scholar
Karrfalt EE (1980) A further comparison of Isoetes roots and stigmarian appendages. Can J Bot 58:2318–2322. https://doi.org/10.1139/b80-268
Article Google Scholar
Kim E, Guak S (2014) Effects of rooting agents and shading treatments on rooting and growth of highbush blueberry hardwood cuttings. Prot Hortic Plant Fact 23:31–38
Article Google Scholar
Liu B, He J, Zeng F et al (2016) Life span and structure of ephemeral root modules of different functional groups from a desert system. New Phytol 211:103–112. https://doi.org/10.1111/nph.13880
CAS Article PubMed Google Scholar
Lux A, Morita S, Abe J, Ito K (2005) An improved method for clearing and staining free-hand sections and whole-mount samples. Ann Bot 96:989–996. https://doi.org/10.1093/aob/mci266
Article PubMed PubMed Central Google Scholar
McCormack ML, Dickie IA, Eissenstat DM et al (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518. https://doi.org/10.1111/nph.13363
Article PubMed Google Scholar
McLennan EI (1935) Non-symbiotic development of seedlings of Epacris impressa Labill. New Phytol 34:55–63. https://doi.org/10.1111/j.1469-8137.1935.tb06827.x
Article Google Scholar
Mihaljević S, Salopek-Sondi B (2012) Alanine conjugate of indole-3-butyric acid improves rooting of highbush blueberries. Plant Soil Environ 58:236–241
Article Google Scholar
Ouimette A, Guo D, Hobbie E, Gu J (2013) Insights into root growth, function, and mycorrhizal abundance from chemical and isotopic data across root orders. Plant Soil 367:313–326. https://doi.org/10.1007/s11104-012-1464-4
CAS Article Google Scholar
Palanisamy K, Kumar P (1997) Effect of position, size of cuttings and environmental factors on adventitious rooting in neem (Azadirachta indica A. Juss). For Ecol Manage 98:277–280. https://doi.org/10.1016/S0378-1127(97)00116-3
Article Google Scholar
Perotto S, Martino E, Abbá S, Vallino M (2012) 14 Genetic diversity and functional aspect of ericoid mycorrhizal fungi. In: Hock B (ed) The Mycota. Volume 9 Fungal Associations. Springer, Berlin, pp 255–285
Chapter Google Scholar
Peterson RL, Massicotte HB, Melville LH (2004) Mycorrhizas: anatomy and cell biology. NRC Research Press, Ottawa
Google Scholar
Pregitzer K, DeForest J, Burton AJ et al (2002) Fine root architecture of nine North American trees. Ecol Monogr 72:293–309. https://doi.org/10.1890/0012-9615(2002)072[0293:FRAONN]2.0.CO;2
Article Google Scholar
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org. Accessed 29 Mar 2017
Read D (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374. https://doi.org/10.1006/anbo.1996.0044
CAS Article Google Scholar
Scagel CF, Wgner A, Winiarski P (2005a) Frequency and intensity of root colonization by ericoid mycorrhizal fungi in nursery production of blueberry plants. Small Fruit Rev 4:95–112. https://doi.org/10.1300/J301v04n04_10
Article Google Scholar
Scagel CF, Wgner A, Winiarski P (2005b) Inoculation with ericoid mycorrhizal fungi alters root colonization and growth in nursery production of blueberry plants from tissue culture and cuttings. Small Fruit Rev 4:113–135. https://doi.org/10.1300/J301v04n04_11
Article Google Scholar
Seago JL, Fernando DD (2013) Anatomical aspects of angiosperm root evolution. Ann Bot 112:223–238. https://doi.org/10.1093/aob/mcs266
CAS Article PubMed PubMed Central Google Scholar
Štefančič M, Štampar F, Osterc G (2005) Influence of IAA and IBA on root development and quality of Prunus “GiSelA 5” leafy cuttings. HortScience 40:2052–2055
Google Scholar
Tawa Y, Takeda H (2015) Which is the best indicator for distinguishing between fine roots with primary and secondary development in Cryptomeria japonica D. Don: Diameter, branching order, or protoxylem groups? Plant Root 9:79–84. https://doi.org/10.3117/plantroot.9.79
Article Google Scholar
Valenzuela-Estrada LR, Vera-Caraballo V, Ruth LE, Eissenstat DM (2008) Root anatomy, morphology, and longevity among root orders in Vaccinium corymbosum (Ericaceae). Am J Bot 95:1506–1514. https://doi.org/10.3732/ajb.0800092
Article PubMed Google Scholar
Vercambre G, Doussan C, Pages L et al (2002) Influence of xylem development on axial hydraulic conductance within Prunus root systems. Trees 16:479–487. https://doi.org/10.1007/s00468-002-0190-6
Article Google Scholar
Wei X, Chen J, Zhang C, Pan D (2016) A new Oidiodendron maius strain isolated from Rhododendron fortunei and its effects on nitrogen uptake and plant growth. Front Microbiol 7:1–11. https://doi.org/10.3389/fmicb.2016.01327
Google Scholar
Wells CE, Eissenstat DM (2001) Marked differences in survivorship among apple roots of different diameters. Ecology 82:882–892. https://doi.org/10.1890/0012-9658(2001)082[0882:MDISAA]2.0.CO;2
Article Google Scholar
Wells CE, Eissenstat DM (2003) Beyond the roots of young seedlings: The influence of age and order on fine root physiology. J Plant Growth Regul 21:324–334. https://doi.org/10.1007/s00344-003-0011-1
Article Google Scholar
Wilcox H (1962) Growth studies of the root of incense cedar, Libocedrus decurrens. II. Morphological features of the root system and growth behavior. Am J Bot 49:237–245
Article Google Scholar
Wu Y, Deng Y, Zhang J et al (2013) Root size and soil environments determine root lifespan: evidence from an alpine meadow on the Tibetan Plateau. Ecol Res 28:493–501. https://doi.org/10.1007/s11284-013-1038-9
CAS Article Google Scholar
Xia M, Guo D, Pregitzer KS (2010) Ephemeral root modules in Fraxinus mandshurica. New Phytol 188:1065–1074. https://doi.org/10.1111/j.1469-8137.2010.03423.x
Article PubMed Google Scholar
Zadworny M, Eissenstat DM (2011) Contrasting the morphology, anatomy and fungal colonization of new pioneer and fibrous roots. New Phytol 190:213–221. https://doi.org/10.1111/j.1469-8137.2010.03598.x
Article PubMed Google Scholar

Download references

Author information

Authors and Affiliations

United Graduate School of Agricultural Science, Tokyo University of Agriculture and Technology, Saiwai-cho, 3-5-8, Fuchu, Tokyo, Japan
Takashi Baba
Faculty of Agriculture, Tokyo University of Agriculture and Technology, Saiwai-cho, 3-5-8, Fuchu, Tokyo, Japan
Satoshi Nakaba & Ryo Funada
Faculty of Agriculture Field Science Center, Tokyo University of Agriculture and Technology, Saiwai-cho, 3-5-8, Fuchu, Tokyo, Japan
Satoshi Noma & Takuya Ban

Authors

Takashi Baba
View author publications
You can also search for this author in PubMed Google Scholar
Satoshi Nakaba
View author publications
You can also search for this author in PubMed Google Scholar
Satoshi Noma
View author publications
You can also search for this author in PubMed Google Scholar
Ryo Funada
View author publications
You can also search for this author in PubMed Google Scholar
Takuya Ban
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takuya Ban.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 957 KB)

Supplementary material 2 (PDF 54 KB)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Baba, T., Nakaba, S., Noma, S. et al. Heterorhizy and fine root architecture of rabbiteye blueberry (Vaccinium virgatum) softwood-cuttings. J Plant Res 131, 271–284 (2018). https://doi.org/10.1007/s10265-017-1000-y

Download citation

Received: 01 September 2017
Accepted: 09 November 2017
Published: 22 December 2017
Issue Date: March 2018
DOI: https://doi.org/10.1007/s10265-017-1000-y

Keywords

Hair root
Heterorhizy
Individual root
Protoxylem group
Root morphology
Vaccinium virgatum Ait.