Is root nutrient uptake a modular function? A test using Solidago canadensis

Abstract

Plant roots have been recognized to be modular, and a third order root cluster has been proposed to be the basic root module unit based upon the life cycle. This experiment examines root modularity of the nutrient-uptake function using stable isotope ¹⁵N. Solidago canadensis root clusters of second or third orders—from the same third or fourth order roots, respectively—were treated with ¹⁵NH₄ ¹⁵NO₃, NH₄NO₃, and de-ionized water for 15 and 180 min. The δ¹⁵N values of the root clusters were then analyzed and compared. The δ¹⁵N values of ¹⁵N-treated root clusters of both second and third orders were hundreds of times higher than that of the ¹⁵N untreated root clusters. However, the differences of the δ¹⁵N values among ¹⁵N untreated root clusters (though expressed some significant variations), did not indicate the ¹⁵N shared by the sister root clusters came from a common higher-order root. These results demonstrated functional modularity of root nutrient uptake, revealed a second order root, perhaps even a first order root to be a base module unit in terms of root nutrient uptake. The results also suggested that the concept of root modularity is function-specific. This experiment further revealed the importance of treatment timing in stabilizing the internal ¹⁵N/¹⁴N ratio in roots and avoiding top-down transportation of ¹⁵N back into roots to secure unbiased measurements.

Keywords

Modularity / Root module / Nitrogen uptake / Solidago canadensis / ¹⁵N

References

[1] Bateman AS, Kelly SD. Fertilizer nitrogen isotope signatures. Isot Environ Health Stud, 2007, 43: 237-247.

[2] Bedard-Haughn AJ, Van G, Van KC. Tracing ¹⁵N through landscapes: potential uses and precautions. J Hydrol, 2003, 272: 175-190.

[3] Bradshaw A. Csapari EW, Thoday JM. Evolutionary significance of phenotypic plasticity in plants. Advances in genetics. 1965, New York: Academic, 115 151

[4] Campbell B, Grime J. A comparative study of plant responsiveness to the duration of episodes of mineral nutrient enrichment. N Phytol, 1989, 112: 261-267.

[5] De Kroon H, Visser EJW, Huber H, Mommer L, Hutchings MJ. A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant Cell Environ, 2009, 32: 704-712.

[6] Einsmann JC, Jones RH, Mou PP, Mitchell AJ. Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms. J Ecol, 1999, 87: 609-619.

[7] Eissenstat DM, Yanai RD. Begon M, Fitter AH. The ecology of root lifespan. Advances in ecological research. 1997, San Diego: Academic, 2 120

[8] Fisher DB, Oparka KJ. Post-phloem transport: principles and problems. J Exp Bot, 1996, 47: 1141-1154.

[9] Fitter A. Caldwell MM, Pearcy RW. Architecture and biomass allocation as components of the plastic response of root systems to soil heterogeneity. Exploitation of environmental heterogeneity by plants—ecophysiological processes above- and belowground. 1994, San Diego: Academic, 305 323

[10] Fitter A, Hay R. Environmental physiology of plants. 1987, San Diego: Academic

[11] Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z. Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. N Phytol, 2008, 180: 673-683.

[12] Harper JL. Population biology of plants. 1977, New York: Academic

[13] Hasegawa S, Koba K, Tayasu I, Takeda H, Haga H. Carbon autonomy of reproductive shoots of Siberian alder Alnus hirsuta var. sibirica. J Plant Res, 2003, 116: 183-188.

[14] Hodge A. The plastic plant: root responses to heterogeneous supplies of nutrients. N Phytol, 2004, 162: 9-24.

[15] Hu F, Mou PP, Weiner J, Li S. Contrasts between whole-plant and local nutrient levels determine root growth and death in Ailanthus altissima Simaroubaceae. Am J Bot, 2014, 101: 812-819.

[16] Hutchings M, de Kroon H. Foraging in plants: the role of morphological plasticity in resource acquisition. Adv Ecol Res, 1994, 25: 159-238.

[17] Kawamura K. A conceptual framework for the study of modular responses to local environmental heterogeneity within the plant crown and a review of related concepts. Ecol Res, 2010, 25: 733-744.

[18] Larcher W. Plant physiological ecology, 1995 3 Berlin: Springer

[19] Marschner H, Kirkby E, Cakmak I. Effect of mineral nutritional status on shoot–root partitioning of photoassimilates and cycling of mineral nutrients. J Exp Bot, 1996, 47: 1255-1263.

[20] Mou PP, Jones RH, Tan Z, Bao Z, Chen H. Morphological and physiological plasticity of plant roots when nutrients are both spatially and temporally heterogeneous. Plant Soil, 2013, 364: 373-384.

[21] Peel AJ. Transport of nutrients in plants. 1974, London: Butterworth and Co. Publishers Ltd.

[22] Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL. Fine root architecture of nine North American trees. Ecol Monogr, 2002, 72: 293-309.

[23] Preston KA, Ackerly DD. Pigliucci M, Preston K. The evolution of allometry in modular organisms. Phenotypic integration: studying the ecology and evolution of complex phenotypes. 2004, Oxford: Oxford University Press, 80 106

[24] Prévost MF. Tomlinson PB, Zimmerman MH. Modular construction and its distribution in tropical woody plants. Tropical trees as living systems. 1978, Cambridge: Cambridge University Press, 223 231

[25] Rivaie AA. The effects of understory vegetation on P availability in Pinus radiata forest stands: a review. J For Res, 2014, 25(3): 489-500.

[26] Robert HS, Friml J. Auxin and other signals on the move in plants. Nat Chem Biol, 2009, 5: 325-332.

[27] Simpson RJ, Lambers H, Dalling M. Kinetin application to roots and its effect on uptake, translocation and distribution of nitrogen in wheat Triticum aestivum grown with a split root system. Physiol Plant, 1982, 56: 430-435.

[28] Wang L, Mou PP, Jones RH. Nutrient foraging via physiological and morphological plasticity in three plant species. Can J For Resour, 2006, 36: 164-173.

[29] White J. The plant as a metapopulation. Annu Rev Ecol Syst, 1979, 10: 109-145.

[30] Xia M, Guo D, Pregitzer KS. Ephemeral root modules in Fraxinus mandshurica. N Phytol, 2010, 188: 1065-1074.