Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Shifts in biomass and nitrogen allocation of tree seedlings in response to root-zone temperature

Suzy Y. Rogiers A B C , Jason P. Smith B , Bruno P. Holzapfel A B and Gurli L. Nielsen B
+ Author Affiliations
- Author Affiliations

A NSW Department of Primary Industries, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia.

B Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia.

C Corresponding author. Email: suzy.rogiers@dpi.nsw.gov.au

Australian Journal of Botany 62(3) 205-216 https://doi.org/10.1071/BT14071
Submitted: 15 April 2014  Accepted: 26 May 2014   Published: 27 June 2014

Abstract

Root-zone warming of trees can result in an increase in biomass production but the mechanisms for this increase may differ between evergreen and deciduous species. The leaf gas exchange, carbohydrate and nitrogen (N) partitioning of two Australian evergreens, Acacia saligna and Eucalyptus cladocalyx, were compared to the deciduous Populus deltoides and Acer negundo after exposure to cool or warm soil during spring. The warm treatment stimulated aboveground biomass production in all four species; however, the form of this increase was species dependent. Compared with the evergreens, soluble sugars were mobilised from the above- and belowground components to a greater extent in the deciduous species, especially during root-zone warming. Photosynthesis, stomatal conductance and transpiration were increased in the warm soil treatment for the two evergreens and P. deltoides only. In P. deltoides and A. saligna the new fine roots contained greater starch concentrations when grown in warm soil but only in A. negundo was new root growth greater. Compared with the other three species, the leguminous A. saligna contained the highest N and most of this was concentrated in the phyllodes of warmed plants with no apparent mobilisation from the existing biomass. In the other evergreen, E. cladocalyx, the existing leaves and stems were a N source for new growth, while in the two deciduous species N was derived from the woody components and structural roots. These data show that the carbohydrate movement and N partitioning patterns in response to soil warming differ between perennial and deciduous plants and are likely responsible for the different forms of biomass accumulation in each of these species.

Additional keywords: biomass partitioning, box elder, cottonwood, soil temperature, sugar gum, wattle.


References

Barnet YM, Catt PC (1991) Distribution and characteristics of root-nodule bacteria isolated from Australian Acacia spp. Plant and Soil 135, 109–120.
Distribution and characteristics of root-nodule bacteria isolated from Australian Acacia spp.Crossref | GoogleScholarGoogle Scholar |

Bassirirad H, Caldwell MM, Bilbrough C (1993) Effects of soil temperature and nitrogen status on kinetics of 15NO3 − uptake by roots of field-grown Agropyron desertorum (Fisch. ex Link) Schult. New Phytologist 123, 485–489.
Effects of soil temperature and nitrogen status on kinetics of 15NO3 uptake by roots of field-grown Agropyron desertorum (Fisch. ex Link) Schult.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltFKgt74%3D&md5=9329a8ac041bae9a155f2e19c48f06efCAS |

Benzioni A, Dunstone RL (1988) Effect of air and soil temperature on water balance of jojoba growing under controlled conditions. Physiologia Plantarum 74, 107–112.
Effect of air and soil temperature on water balance of jojoba growing under controlled conditions.Crossref | GoogleScholarGoogle Scholar |

Berndt M-L, McCully ME, Canny MJ (1999) Is xylem embolism and refilling involved in the rapid wilting and recovery of plants following root cooling and rewarming? A cryo-microscope investigation. Plant Biology 1, 506–515.
Is xylem embolism and refilling involved in the rapid wilting and recovery of plants following root cooling and rewarming? A cryo-microscope investigation.Crossref | GoogleScholarGoogle Scholar |

Boughton VH (1986) Phyllode structure, taxonomy and distribution in some Australian acacias. Australian Journal of Botany 34, 663–674.
Phyllode structure, taxonomy and distribution in some Australian acacias.Crossref | GoogleScholarGoogle Scholar |

Cai T, Dang Q-L (2002) Effects of soil temperature on parameters of a coupled photosynthesis–stomatal conductance model. Tree Physiology 22, 819–828.
Effects of soil temperature on parameters of a coupled photosynthesis–stomatal conductance model.Crossref | GoogleScholarGoogle Scholar | 12184971PubMed |

Chapin F, Schulze E-D, Mooney H (1990) The ecology and economics of storage in plants. Annual Review of Ecology and Systematics 21, 423–447.
The ecology and economics of storage in plants.Crossref | GoogleScholarGoogle Scholar |

Cherbuy B, Joffre R, Gillon D, Rambal S (2001) Internal remobilization of carbohydrates, lipids, nitrogen and phosphorus in the Mediterranean evergreen oak Quercus ilex. Tree Physiology 21, 9–17.
Internal remobilization of carbohydrates, lipids, nitrogen and phosphorus in the Mediterranean evergreen oak Quercus ilex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtVegs7o%3D&md5=c94a2e4778788254a6fd2babd76f28f6CAS | 11260819PubMed |

Cline GC (1991) Apical dominance. Botanical Review 57, 318–358.
Apical dominance.Crossref | GoogleScholarGoogle Scholar |

Coleman GD, Ernst THH, Chen SG, Fuchigami H (1991) Photoperiod control of poplar bark storage protein accumulation. Plant Physiology 96, 686–692.
Photoperiod control of poplar bark storage protein accumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFSksLg%3D&md5=8e36dac19e52148bd16769a7dae7bcc4CAS | 16668243PubMed |

Erice G, Irigoyen JJ, Pérez P, Martínez-Carrasco R, Sánchez-Díaz M (2006) Effect of elevated CO2, temperature and drought on photosynthesis of nodulated alfalfa during a cutting regrowth cycle. Physiologia Plantarum 126, 458–468.
Effect of elevated CO2, temperature and drought on photosynthesis of nodulated alfalfa during a cutting regrowth cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVehurw%3D&md5=a99492e03326c0705a12e4f7cbd2d153CAS |

Fennell A, Markhart AH (1998) Rapid acclimation of root hydraulic conductivity to low temperature. Journal of Experimental Botany 49, 879–884.
Rapid acclimation of root hydraulic conductivity to low temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjs1Sju7Y%3D&md5=a888a4dc3379b3a8a70aed7c49fd805fCAS |

Field SK, Smith JP, Holzapfel BP, Hardie WJ, Emery RJN (2009) Grapevine response to soil temperature: xylem cytokinins and carbohydrate reserve mobilization from budbreak to anthesis. American Journal of Enology and Viticulture 60, 164–172.

Foster JR (1992) Photosynthesis and water relations of the floodplain tree, boxelder (Acer negundo L.). Tree Physiology 11, 133–149.
Photosynthesis and water relations of the floodplain tree, boxelder (Acer negundo L.).Crossref | GoogleScholarGoogle Scholar | 14969957PubMed |

Gleadow RM, Woodrow IE (2002) Defense chemistry of cyanogenic Eucalyptus cladocalyx seedlings is affected by water supply. Tree Physiology 22, 939–945.
Defense chemistry of cyanogenic Eucalyptus cladocalyx seedlings is affected by water supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xns1emsbw%3D&md5=f5473b16701f9d79c9ea9b1bc527f3cbCAS | 12204850PubMed |

Goodwin PB, Gollnow BI, Letham DS (1978) Phytohormones and growth correlations. In ‘Phytohormones and related compounds: a comprehensive treatise. Vol. 2’. (Eds D Letham, P Goodwin, T Higgins) pp. 215–249. (Elsevier-North Holland Biomedical Press: Amsterdam)

Greer DH, Wünsche JN, Norling CL, Wiggins HN (2006) Root-zone temperatures affect phenology of bud break, flower cluster development, shoot extension growth and gas exchange of ‘Braeburn’ (Malus domestica) apple trees. Tree Physiology 26, 105–111.
Root-zone temperatures affect phenology of bud break, flower cluster development, shoot extension growth and gas exchange of ‘Braeburn’ (Malus domestica) apple trees.Crossref | GoogleScholarGoogle Scholar | 16203720PubMed |

He J, Lee SK (2001) Relationship among photosynthesis, ribulose-1,5-bisphosphate carboxylase (Rubisco) and water relations of the subtropical vegetable Chinese broccoli grown in the tropics by manipulation of root-zone temperature. Environmental and Experimental Botany 46, 119–128.
Relationship among photosynthesis, ribulose-1,5-bisphosphate carboxylase (Rubisco) and water relations of the subtropical vegetable Chinese broccoli grown in the tropics by manipulation of root-zone temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmt1yjs7Y%3D&md5=561bcc5ec1c827e0f8b8abfe2746a21bCAS |

Hennessy KJ, Fawcett R, Kirono D, Mpelasoka F, Jones D, Bathols J, Whetton P, Stafford Smith M, Howden M, Mitchell C, Plummer N (2008) ‘An assessment of the impact of climate change on the nature and frequency of exceptional climatic events.’ (Department of Agriculture, Fisheries and Forestry)

Holmes PM, Cowling RM (1997) The effects of invasion by Acacia saligna on the guild structure and regeneration capabilities of South African fynbos shrublands. Journal of Applied Ecology 34, 317–332.
The effects of invasion by Acacia saligna on the guild structure and regeneration capabilities of South African fynbos shrublands.Crossref | GoogleScholarGoogle Scholar |

Kaufmann MR (1975) Leaf water stress in Engelmann spruce. Influence of the root and shoot environments. Plant Physiology 56, 841–844.
Leaf water stress in Engelmann spruce. Influence of the root and shoot environments.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhtFGrug%3D%3D&md5=33ee3cfdb9a84550460a9edeaf9e3307CAS | 16659406PubMed |

Kramer PJ, Boyer JS (1995) ‘Water relations of plants and soil.’ (Academic Press: San Diego, CA)

Landhäusser SM, DesRochers A, Lieffers VJ (2001) A comparison of growth and physiology in Picea glauca and Populus tremuloides at different soil temperatures. Canadian Journal of Forest Research 31, 1922–1929.
A comparison of growth and physiology in Picea glauca and Populus tremuloides at different soil temperatures.Crossref | GoogleScholarGoogle Scholar |

Lopushinsky W, Kaufmann MR (1984) Effects of cold soil on water relations and spring growth of Douglas-fir seedlings. Forest Science 30, 628–634.

MacDonald NW, Zak DR, Pregitzer KS (1995) Temperature effects on kinetics of microbial respiration and net nitrogen and sulfur mineralization. Soil Science Society of America Journal 59, 233–240.
Temperature effects on kinetics of microbial respiration and net nitrogen and sulfur mineralization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtlelt7c%3D&md5=9929c8716cdd992b79438de0853ebb09CAS |

Marshall JD, Waring RH (1985) Predicting fine root production and turnover by monitoring root starch and soil temperature. Canadian Journal of Forest Research 15, 791–800.
Predicting fine root production and turnover by monitoring root starch and soil temperature.Crossref | GoogleScholarGoogle Scholar |

Marsudi NDS, Glenn AR, Dilworth MJ (1999) Identification and characterization of fast- and slow-growing root nodule bacteria from South-Western Australian soils able to nodulate Acacia saligna. Soil Biology & Biochemistry 31, 1229–1238.
Identification and characterization of fast- and slow-growing root nodule bacteria from South-Western Australian soils able to nodulate Acacia saligna.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlyjurg%3D&md5=c81d983c41b8eff4727197cd27fdb2c5CAS |

Monk CD (1966) An ecological significance of evergreenness. Ecology 47, 504–505.
An ecological significance of evergreenness.Crossref | GoogleScholarGoogle Scholar |

Mora F, Gleadow R, Perret S, Scapim C (2009) Genetic variation for early flowering, survival and growth in sugar gum (Eucalyptus cladocalyx F. Muell) in southern Atacama Desert. Euphytica 169, 335–344.
Genetic variation for early flowering, survival and growth in sugar gum (Eucalyptus cladocalyx F. Muell) in southern Atacama Desert.Crossref | GoogleScholarGoogle Scholar |

Reddell P, Bowen GD, Robson AD (1985) The effects of soil temperature on plant growth, nodulation and nitrogen fixation in Casuarina cunninghamiana Miq. New Phytologist 101, 441–450.
The effects of soil temperature on plant growth, nodulation and nitrogen fixation in Casuarina cunninghamiana Miq.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XjtFyntA%3D%3D&md5=6a1ad37d55c203a51099f4f8e3451ef0CAS |

Rogiers SY, Clarke SJ (2013) Nocturnal and daytime stomatal conductance respond to root-zone temperature in ‘Shiraz’ grapevines. Annals of Botany 111, 433–444.
Nocturnal and daytime stomatal conductance respond to root-zone temperature in ‘Shiraz’ grapevines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtV2ksb4%3D&md5=294bc5cf07d632688502b73ca6ed4334CAS | 23293018PubMed |

Rogiers SY, Hardie WJ, Smith JP (2011a) Stomatal density of grapevine leaves (Vitis vinifera L.) responds to soil temperature and atmospheric carbon dioxide. Australian Journal of Grape and Wine Research 17, 147–152.
Stomatal density of grapevine leaves (Vitis vinifera L.) responds to soil temperature and atmospheric carbon dioxide.Crossref | GoogleScholarGoogle Scholar |

Rogiers SY, Smith JP, Holzapfel BP, Hardie WJ (2011b) Soil temperature moderates grapevine carbohyrate reserves after bud break and conditions fruit set responses to photoassimilatory stress. Functional Plant Biology 38, 899–909.
Soil temperature moderates grapevine carbohyrate reserves after bud break and conditions fruit set responses to photoassimilatory stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlagu7jL&md5=1956d6bc6036c09cfac4f50927006f64CAS |

Sauter JJ, Van Cleve B (1992) Seasonal variation of amino acids in the xylem sap of Populus × canadensis and its relation to protein body remobilization. Trees 7, 26–32.
Seasonal variation of amino acids in the xylem sap of Populus × canadensis and its relation to protein body remobilization.Crossref | GoogleScholarGoogle Scholar |

Saxe H, Cannell MGR, Johnsen Ø, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytologist 149, 369–399.
Tree and forest functioning in response to global warming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1ansrk%3D&md5=1841c52cc9c2c2f3d31509918a9e5eefCAS |

Schoch P-G, Jacques R, Lecharny A, Sibi M (1984) Dependence of the stomatal index on environment factors during stomatal differentiation in leaves of Vigna sinensis L. II. Effect of different light quality. Journal of Experimental Botany 35, 1405–1409.
Dependence of the stomatal index on environment factors during stomatal differentiation in leaves of Vigna sinensis L. II. Effect of different light quality.Crossref | GoogleScholarGoogle Scholar |

Schwarz PA, Fahey TJ, Dawson TE (1997) Seasonal air and soil temperature effects on photosynthesis in red spruce (Picea rubens) saplings. Tree Physiology 17, 187–194.
Seasonal air and soil temperature effects on photosynthesis in red spruce (Picea rubens) saplings.Crossref | GoogleScholarGoogle Scholar | 14759873PubMed |

Skene KGM, Kerridge GH (1967) Effect of root temperature on cytokinin activity in root exudate of Vitis vinifera L. Plant Physiology 42, 1131–1139.
Effect of root temperature on cytokinin activity in root exudate of Vitis vinifera L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXltVOmt7k%3D&md5=d3f1dcf80a1126b3bc5acaa3c11c43a8CAS |

Stock WD, Wienand KT, Baker AC (1995) Impacts of invading N2-fixing Acacia species on patterns of nutrient cycling in two Cape ecosystems: evidence from soil incubation studies and 15N natural abundance values. Oecologia 101, 375–382.
Impacts of invading N2-fixing Acacia species on patterns of nutrient cycling in two Cape ecosystems: evidence from soil incubation studies and 15N natural abundance values.Crossref | GoogleScholarGoogle Scholar |

Stone PJ, Sorensen IB, Jamieson PD (1999) Effect of soil temperature on phenology, canopy development, biomass and yield of maize in a cool-temperature climate. Field Crops Research 63, 169–178.

Stoneman GL, Dell B (1993) Growth of Eucalyptus marginata (Jarrah) seedlings in a greenhouse in response to shade and soil temperature. Tree Physiology 13, 239–252.
Growth of Eucalyptus marginata (Jarrah) seedlings in a greenhouse in response to shade and soil temperature.Crossref | GoogleScholarGoogle Scholar | 14969882PubMed |

Tromp J (1983) Nutrient reserves in root of fruit trees, in particular carbohydrates and nitrogen. Plant and Soil 71, 401–413.
Nutrient reserves in root of fruit trees, in particular carbohydrates and nitrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXkvVGjt78%3D&md5=af41ab3ac0162c8dee77417c9f04da9eCAS |

Tromp J (1996) Sylleptic shoot formation in young apple trees exposed to various soil temperature and air humidity regimes in three successive periods of the growing season. Annals of Botany 77, 63–70.
Sylleptic shoot formation in young apple trees exposed to various soil temperature and air humidity regimes in three successive periods of the growing season.Crossref | GoogleScholarGoogle Scholar |

Trueman SJ, McMahon TV, Bristow M (2013) Production of Eucalyptus cloeziana cuttings in response to stock plant temperature. Journal of Tropical Forest Science 25, 60–69.

van Gestel NC, Schwilk DW, Tissue DT, Zak JC (2011) Reductions in daily soil temperature variability increase soil microbial biomass C and decrease soil N availability in the Chihuahuan Desert: potential implications for ecosystem C and N fluxes. Global Change Biology 17, 3564–3576.
Reductions in daily soil temperature variability increase soil microbial biomass C and decrease soil N availability in the Chihuahuan Desert: potential implications for ecosystem C and N fluxes.Crossref | GoogleScholarGoogle Scholar |

Wan X, Landhäusser SM, Zwiazek JJ, Lieffers VJ (1999) Root water flow and growth of aspen (Populus tremuloides) at low root temperatures. Tree Physiology 19, 879–884.
Root water flow and growth of aspen (Populus tremuloides) at low root temperatures.Crossref | GoogleScholarGoogle Scholar | 10562405PubMed |

Wan X, Landhäusser SM, Zwiazek JJ, Lieffers VJ (2004) Stomatal conductance and xylem sap properties of aspen (Populus tremuloides) in response to low soil temperature. Physiologia Plantarum 122, 79–85.
Stomatal conductance and xylem sap properties of aspen (Populus tremuloides) in response to low soil temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFeht7g%3D&md5=c301bad366206bf5b2360c3aaaa66e10CAS |

Wendler R, Carvalho PO, Pereira JS, Millard P (1995) Role of nitrogen remobilization from old leaves for new leaf growth of Eucalyptus globulus seedlings. Tree Physiology 15, 679–683.
Role of nitrogen remobilization from old leaves for new leaf growth of Eucalyptus globulus seedlings.Crossref | GoogleScholarGoogle Scholar | 14966002PubMed |

Woodrow IE, Slocum DJ, Gleadow RM (2002) Influence of water stress on cyanogenic capacity in Eucalyptus cladocalyx. Functional Plant Biology 29, 103–110.
Influence of water stress on cyanogenic capacity in Eucalyptus cladocalyx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVCiu7Y%3D&md5=944e2b1955e4d077e39b97d0586975b3CAS |

Woodward FI, Kelly CK (1995) The influences of CO2 concentration on stomatal density. New Phytologist 131, 311–327.
The influences of CO2 concentration on stomatal density.Crossref | GoogleScholarGoogle Scholar |

Wu S, Jansson P-E, Kolari P (2012) The role of air and soil temperature in the seasonality of photosynthesis and transpiration in a boreal Scots pine ecosystem. Agricultural and Forest Meteorology 156, 85–103.
The role of air and soil temperature in the seasonality of photosynthesis and transpiration in a boreal Scots pine ecosystem.Crossref | GoogleScholarGoogle Scholar |

Yelenik SG, Stock WD, Richardson DM (2004) Ecosystem level impacts of invasive Acacia saligna in the South African Fynbos. Restoration Ecology 12, 44–51.
Ecosystem level impacts of invasive Acacia saligna in the South African Fynbos.Crossref | GoogleScholarGoogle Scholar |

Zapata C, Deléens E, Chaillou S, Magné C (2004) Partitioning and mobilization of starch and N reserves in grapevine (Vitis vinifera L.). Journal of Plant Physiology 161, 1031–1040.
Partitioning and mobilization of starch and N reserves in grapevine (Vitis vinifera L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptlOgt74%3D&md5=0e89e2c0b69763592948244ca56fbe72CAS | 15499905PubMed |

Zhang YP, Qiao YX, Zhang YL, Zhou YH, Yu JQ (2008) Effects of root temperature on leaf gas exchange and xylem sap abscisic acid concentrations in six Cucurbitaceae species. Photosynthetica 46, 356–362.
Effects of root temperature on leaf gas exchange and xylem sap abscisic acid concentrations in six Cucurbitaceae species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFaisbbE&md5=dccde9792a62a243890bcdd6da3997b3CAS |

Zhou YH, Yu JQ, Huang LF, Nogués S (2004) The relationship between CO2 assimilation, photosynthetic electron transport and water-water cycle in chill-exposed cucumber leaves under low light and subsequent recovery. Plant, Cell & Environment 27, 1503–1514.
The relationship between CO2 assimilation, photosynthetic electron transport and water-water cycle in chill-exposed cucumber leaves under low light and subsequent recovery.Crossref | GoogleScholarGoogle Scholar |