Variation in the morphology of fine roots in Cryptomeria japonica determined by branch order-based classification
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Abstract
Aims
This study assessed intraspecific variation in morphological traits of the fine root branch orders of Cryptomeria japonica, and identified variation in the diameter of the first three-order roots among species types with mycorrhiza, and the diameter of first-order roots at the family level.
Methods
Diameter, length, and specific root length of branch order roots (up to the fourth-order) were measured in intact fine root systems collected in four C. japonica stands. Relationships between soil chemical properties and morphological traits of the first- to fourth-order roots were investigated. The diameter of roots of 52 tree species reported in previous studies was compared at species types with mycorrhiza and at family level.
Results
The diameter of first-order roots in C. japonica varied by 1.2 times among stands. Negative correlations between soil NH4+ content and specific root length of the second- and third-order roots were observed in C. japonica. The diameter of first- and second-order roots forming arbuscular mycorrhiza in coniferous trees were significantly higher than those of roots forming ectomycorrhiza in coniferous and broadleaf trees. The diameter of first-order roots in Cupressaceae were significantly larger than those of Pinaceae, Sapindaceae, Betulaceae, and Fagaceae.
Conclusions
Clarifying intraspecific variation in morphological traits of C. japonica lower-order roots may contribute to understanding their responses to different site conditions such as soil inorganic nitrogen contents.
Keywords
Absorptive roots Arbuscular mycorrhiza Evolutionary history Root diameter Specific root lengthAbbreviations
- Al
Aluminum
- AM
Arbuscular mycorrhiza
- C
Carbon
- EC
Electrical conductivity
- EM
Ectomycorrhiza
- N
Nitrogen
- NPP
Net primary productivity
- SRL
Specific root length
Notes
Acknowledgements
We appreciate the constructive comments of the editor and three reviewers on the submitted manuscript. We also thank K. Noguchi (Forestry and Forest Product Research Institute, FFPRI) for reading the first draft of the manuscript and providing invaluable comments. We thank M. Takano, Y. Yamaguchi, T. Miyasaka (Nagoya University), T. Okamoto, T. Mizoguchi (FFPRI), and Y. Matsuda (Mie University) for their invaluable suggestions and assistance with fieldwork and laboratory analyses. We thank K. Yamase (Hyogo Prefectural Technology Center for Agriculture, Forestry and Fisheries), T. Kobayashi (Research Institute of Environment, Agriculture and Fisheries, Osaka Prefecture), and H. Fukumoto (The Mie Prefectural Forestry Research Center) for permission to access to the Forest Health-Monitoring Survey Sites of the Forestry Agency of Japan. This study was partly funded by JSPS KAKENHI Grant number 15H04519, 18 J23364 and 19H03011.
Supplementary material
References
- Brunner I, Bakker MR, Björk RG, Hirano Y, Lukac M, Aranda X, Børja I, Eldhuset TD, Helmisaari HS, Jourdan C, Konôpka B, López BC, Pérez CM, Persson H, Ostonen I (2013) Fine- root turnover rates of European forests revisited: an analysis of data from sequential coring and ingrowth cores. Plant Soil 362:357–372Google Scholar
- Brunsfeld SJ, Soltis PA, Soltis DE, Gadek PA, Quinn CJ, Strenge DD, Ranker TA (1994) Phylogenetic relationships among the genera of Taxodiaceae and Cupressaceae: evidence from rbcL sequences. Syst Bot 19:253–262Google Scholar
- Chen W, Zeng H, Eissenstat DM, Guo D (2013) Variation of first-order root traits across climatic gradients and evolutionary trends in geological time. Glob Ecol Biogeogr 22:846–856Google Scholar
- Chen H, Dong Y, Xu T, Wang Y, Wang H, Duan B (2017) Root order-dependent seasonal dynamic in the carbon and nitrogen chemistry of poplar fine roots. New For 48:587–607Google Scholar
- Comas LH, Mueller KE, Taylor LL, Midford PE, Callahan HS, Beerling D (2012) Evolutionary patterns and biogeochemical significance of angiosperm root traits. Int J Plant Sci 173:584–595Google Scholar
- Comas LH, Callahan HS, Midford PE (2014) Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implication for the evolution of below ground strategies. Ecol Evol 4:2979–2990PubMedPubMedCentralGoogle Scholar
- Doi R, Tanikawa T, Miyatani K, Hirano Y (2017) Intraspecific variation in morphological traits of root branch orders in Chamaecyparis obtusa. Plant Soil 416:503–513Google Scholar
- Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:2–60Google Scholar
- Eissenstat DM, Kucharski JM, Zadworny M, Adams TS, Koide RT (2015) Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest. New Phytol 208:114–124Google Scholar
- FAO-UNESCO (1990) Soil map of the world revised legend. FAO, RomeGoogle Scholar
- Finér L, Ohashi M, Noguchi K, Hirano Y (2011a) Fine root production and turnover in forest ecosystems in relation to stand and environmental characteristics. For Ecol Manag 262:2008–2023Google Scholar
- Finér L, Ohashi M, Noguchi K, Hirano Y (2011b) Factors causing variation in fine root biomass in forest ecosystems. For Ecol Manag 261:265–277Google Scholar
- Forest Soil Division (1976) Classification of forest soils in Japan. Bull Gov For Exp Stn 280:1–28 (in Japanese with English summaryGoogle Scholar
- Forestry Agency of Japan (1997) Report for Forest damage-monitoring project by acid deposition (1990–1994), Tokyo (in Japanese)Google Scholar
- Freschet GT, Roumet C (2017) Sampling roots to capture plant and soil functions. Funct Ecol 31:1506–1518Google Scholar
- Fujimaki R, Tateno R, Tokuchi N (2007) Root development across a chronosequence in a Japanese cedar (Cryptomeria japonica D. Don) plantation. J For Res 12:96–102Google Scholar
- Gadek PA, Alpers DL, Heslewood MM, Quinn CJ (2000) Relationships within Cupressaceae sensu lato: a combined morphological and molecular approach. Am J Bot 87:1044–1057PubMedGoogle Scholar
- Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140:450–457Google Scholar
- Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683Google Scholar
- Hirano Y, Mizoguchi T, Brunner I (2007) Root parameters of forest trees as sensitive indicators of acidifying pollutants: a review of research of Japanese forest trees. J For Res 12:134–142Google Scholar
- Hirano Y, Tanikawa T, Makita N (2017) Biomass and morphology of fine roots in eight Cryptomeria japonica stands in soils with different acid-buffering capacities. For Ecol Manag 384:122–131Google Scholar
- Hishi T, Tateno R, Fukushima K, Fujimaki R, Itoh M, Tokuchi N (2017) Changes in the anatomy, morphology and mycorrhizal infection of fine root systems of Cryptomeria japonica in relation to stand ageing. Tree Physiol 37:61–70PubMedGoogle Scholar
- Jia S, Wang Z, Li X, Zhang X, Mclaughlin B (2013) Relationships between root respiration rate and root morphology, chemistry and anatomy in Larix gmelinii and Fraxinus mandshurica. Tree Physiol 33:579–589. https://doi.org/10.1093/treephys/tpt040 CrossRefPubMedGoogle Scholar
- Kawahara T (2014) New group systems based on APG. For Genetic Tree Breed 3:15–22 (in Japanese)Google Scholar
- Kong D, Ma C, Zhang Q, Li L, Chen X, Zeng H, Guo D (2014) Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytol 203:863–872PubMedGoogle Scholar
- Konôpka B, Noguchi K, Sakata T, Konôpková Z (2006) Fine root dynamics in a Japanese cedar (Cryptomeria japonica) plantation throughout the growing season. For Ecol Manag 225:278–286Google Scholar
- Kramer-Walter KR, Laughlin DC (2017) Root nutrient concentration and biomass allocation are more plastic than morphological traits in response to nutrient limitation. Plant Soil 416:539–550Google Scholar
- Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–1310Google Scholar
- Kubisch P, Hertel D, Leuschner C (2015) Do ectomycorrhizal and arbuscular mycorrhizal temperate tree species systematically differ in root order-related fine root morphology and biomass? Front Plant Sci 6:1–12Google Scholar
- Laughlin DC (2014) The intrinsic dimensionality of plant traits and its relevance to community assembly. J Ecol 102:186–193Google Scholar
- Liese R, Alings K, Meier IC (2017) Root branching is a leading root trait of the plant economic spectrum in temperate trees. Front Plant Sci 8:315. https://doi.org/10.3389/fpls.2017.00315 CrossRefPubMedPubMedCentralGoogle Scholar
- Liu B, Li H, Zhu B, Koide RT, Eissenstat DM, Guo D (2015) Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytol 208:125–136Google Scholar
- Ma Z, Guo D, Xu X, Lu M, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO (2018) Evolutionary history resolves global organization of root functional traits. Nature 555:94–97Google Scholar
- Maherali H (2014) Is there an association between root architecture and mycorrhizal growth response? New Phytol 204:192–200PubMedGoogle Scholar
- McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari H-S, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of belowground contributions to terrestrial biosphere processes. New Phytol 207:505–518PubMedGoogle Scholar
- Miyatani K, Mizusawa Y, Okada K, Tanikawa T, Makita N, Hirano Y (2016) Fine root traits in Chamaecyparis obtusa forest soils with different acid buffering capacities. Trees 30:415–429Google Scholar
- Miyatani K, Tanikawa T, Makita N, Hirano Y (2018) Relationships between specific root length and respiration rate of fine roots across stands and seasons in Chamaecyparis obtusa. Plant Soil 423:215–227Google Scholar
- Nagakura J, Kaneko S, Takahashi M, Tange T (2008) Nitrogen promotes water consumption in seedlings of Cryptomeria japonica but not in Chamaecyparis obtusa. For Ecol Manag 255:2533–2541Google Scholar
- Noguchi K, Konôpka B, Satomura T, Kaneko S, Takahashi M (2007) Biomass and production of fine roots in Japanese forests. J For Res 12:83–95Google Scholar
- Noguchi K, Nagakura J, Kaneko S (2013a) Biomass and morphology of fine roots of sugi (Cryptomeria japonica) after 3 years of nitrogen fertilization. Front Plant Sci 4:1–7Google Scholar
- Noguchi K, Nagakura J, Konôpka B, Sakata T, Kaneko S, Takahashi M (2013b) Fine-root dynamics in sugi (Cryptomeria japonica) under manipulated soil nitrogen conditions. Plant Soil 364:159–169Google Scholar
- Ohyama T (1990) Inorganic nitrogen. In: editing committee of experimental methods for plant nutrition (ed) experimental methods for plant nutrition. Hakuyusha, Tokyo, pp 174–179 in JapaneseGoogle Scholar
- Ostonen I, Püttsepp Ü, Biel C, Alberton O, Bakker MR, Lõhmus K, Majdi H, Metcalfe D, Olsthoorn AFM, Pronk A, Vanguelova E, Weih M, Brunner I (2007) Specific root length as an indicator of environmental change. Plant Biosys 141:426–442Google Scholar
- Pregitzer KS, Deforest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine north American trees. Ecol Monogr 72:293–309Google Scholar
- Román-Jordán E, Esteban LG, de Palacios P, Fernández FG (2017) Comparative wood anatomy of the Cupressaceae and correspondence with phylogeny, with special reference to the monotypic taxa. Plant Syst Evol 303:203–219Google Scholar
- Sakata T (2000) Quantification of NO3 −-N in soil extracts using UVabsorption method. Jpn J Environ 42:53–55 (in Japanese)Google Scholar
- Takahashi M, Sakata T, Ishizuka K (2001) Chemical characteristics and acid buffering capacity of surface soils in Japanese forests Water Air Soil Pollut 130:727–732Google Scholar
- Tanikawa T, Sobue A, Hirano Y (2014) Acidification processes in soils with different acid buffering capacity in Cryptomeria japonica and Chamaecyparis obtusa forests over two decades. For Ecol Manag 334:284–292Google 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 Roots 9:79–84Google Scholar
- Wang Z, Guo D, Wang X, Gu J, Mei L (2006) Fine root architec- ture, morphology, and biomass of different branch orders of two Chinese temperate tree species. Plant Soil 288:155–171Google Scholar
- Wang G, Fahey TJ, Xue S, Liu F (2013) Root morphology and architecture respond to N addition in Pinus tabuliformis, West China. Oecologia 171:583–590PubMedGoogle Scholar
- Zadworny M, McCormack ML, Rawlik K, Jagodziński AM (2015) Seasonal variation in chemistry, but not morphology, in roots of Quercus robur growing in different soil types. Tree Physiol 35:644–652PubMedGoogle Scholar
- Zadworny M, McCormack ML, Mucha J, Reich P, Oleksyn J (2016) Scots pine fine roots adjust along a 2000-km latitudinal climatic gradient. New Phytol 212:389–399PubMedGoogle Scholar
- Zadworny M, McCormack ML, Żytkowiak R, Karolewski P, Mucha J, Oleksyn J (2017) Patterns of structural and defense investments in fine roots of scots pine (Pinus sylvestris L.) across a strong temperature and latitudinal gradient in Europe. Glob Chang Biol 23:1218–1231PubMedGoogle Scholar