15N partitioning in tomato: vascular constraints versus tissue demand
Amy E. Zanne A B E , Steven S. Lower A C , Zoe G. Cardon D and Colin M. Orians AA Department of Biology, Tufts University, Medford, MA 02155, USA.
B Department of Biology, Macquarie University, North Ryde, NSW 2109, Australia.
C Department of Nematology, University of California Davis, Davis, CA 95616, USA.
D Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269, USA.
E Corresponding author. Email: aezanne@yahoo.com
F This paper originates from a presentation at ECOFIZZ 2005, North Stradbroke Island, Queensland, Australia, November 2005.
Functional Plant Biology 33(5) 457-464 https://doi.org/10.1071/FP05299
Submitted: 12 December 2005 Accepted: 24 February 2006 Published: 2 May 2006
Abstract
Allocation of root-derived resources is influenced by tissue demand; however, vascular pathways mediate resource flow from roots to shoots. In vascularly constrained plants (i.e. sectored plants), effects of vascular connections likely limit homogenous resource delivery, especially when environmental resource distribution is patchy. Here, we quantify relative roles of vascular connections, demands by different leaves (i.e. by leaf age and size), and molecule size of transported N compounds (effective sectoriality: nitrate v. ammonium) on allocation of 15N in the sectored tomato (Solanum lycopersicum L.). Vascular connections were the strongest predictor of both accumulation (amount per leaf; P<0.0001) and δ (estimate of concentration; P<0.0001) 15N values in mature leaves, but young expanding leaves did not show such dramatically sectored uptake (accumulation: P=0.0685; δ: P=0.0455), suggesting that sectoriality is less strong in young expanding tissue, especially in the youngest leaf. In patchy environments sectoriality, then, should have large consequences for the ability of a plant to allocate resources in mature tissue; however, young leaves do not appear to experience such strong vascular constraints when building new tissue.
Keywords: ammonium, developmental state, effective sectoriality, 15N isotope, nitrate, patchy resources, Solanum, vascular connections.
Acknowledgments
We thank Ben Babst, Brian Brannigan, Vit Gloser and Margaret Van Vuuren for assistance with setup, methods and helpful discussions, David Warton for assistance with statistical analyses, and Vit Gloser, Lou Santiago, and two anonymous reviewers for helpful comments on earlier versions of this manuscript. This project was supported by grants from The Andrew Mellon Foundation to CMO and, in part, to ZGC.
Andrews M
(1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant, Cell & Environment 9, 511–529.
Bledsoe TM, Orians CM
(2006) Vascular pathways constrain 13C accumulation in large root sinks of Lycopersicon esculentum (Solanaceae). American Journal of Botany In press
,
Bloom AJ
(1988) Ammonium and nitrate as nitrogen sources for plant growth. ISI Atlas of Science: Animal and Plant Sciences 1, 1–302.
Choat B,
Ball M,
Luly J, Holtum J
(2003) Pit membrane and water stress-induced cavitation in four co-existing dry rainforest tree species. Plant Physiology 131, 41–48.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dawson TE,
Mambelli S,
Plamboeck AH,
Templer PH, Tu KP
(2002) Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33, 507–559.
| Crossref | GoogleScholarGoogle Scholar |
Dimond AE
(1966) Pressure and flow relations in vascular bundles of the tomato plant. Plant Physiology 41, 119–131.
Evans RD,
Bloom AJ,
Sukrapanna SS, Ehleringer JR
(1996) Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. Cv. T–5) grown under ammonium or nitrate nutrition. Plant, Cell & Environment 19, 1317–1323.
Gao Z,
Sagi M, Lips H
(1996) Assimilate allocation priority as affected by nitrogen compounds in the xylem sap of tomato. Plant Physiology and Biochemistry 34, 807–815.
Hay MJM, Sackville Hamilton NR
(1996) Influence of xylem vascular architecture on the translocation of phosphorous from nodal roots in a genotype of Trifolium repens during undisturbed growth. New Phytologist 132, 575–582.
Jones CG,
Hopper RF,
Coleman JS, Krischik VA
(1993) Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93, 452–456.
| Crossref | GoogleScholarGoogle Scholar |
Khan AA, Sagar GR
(1966) Distribution of 13C-labelled products of photosynthesis during the commercial life of the tomato crop. Annals of Botany 30, 727–743.
Lopes MS,
Nogués S, Araus J
(2004) Nitrogen source and water regime effects on barley photosynthesis and isotope signature. Functional Plant Biology 31, 995–1003.
| Crossref | GoogleScholarGoogle Scholar |
Lorenz H
(1976) Nitrate, ammonium and amino acids in the bleeding sap of tomato plants in relation to form and concentration of nitrogen in the medium. Plant and Soil 45, 169–175.
| Crossref | GoogleScholarGoogle Scholar |
Orians CM, Jones CG
(2001) Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability. Oikos 94, 493–504.
| Crossref | GoogleScholarGoogle Scholar |
Orians CM,
Pomerleau J, Ricco R
(2000) Vascular architecture generates fine scale variation in the systemic induction of proteinase inhibitors in tomato. Journal of Chemical Ecology 26, 471–485.
| Crossref | GoogleScholarGoogle Scholar |
Orians CM,
Ardon M, Mohammad BA
(2002) Vascular architecture and patchy nutrient availability generate within-plant heterogeneity in plant traits important to herbivores. American Journal of Botany 89, 270–278.
Orians CM,
Van Vuuren MM,
Harris NL,
Babst BA, Ellmore GS
(2004) Differential sectoriality in long distance transport in temperate tree species: evidence from dye flow, 15N transport, and vessel element pitting. Trees 18, 501–509.
| Crossref |
Sano YZ
(2004) Intervascular pitting across the annual ring boundary in Betula platyphylla var. japonica and Fraxinus manshurica var. japonica. IAWA Journal 25, 129–140.
Schittko U, Baldwin IT
(2003) Constraints to herbivore-induced systemic responses: bidirectional signaling along orthostichies in Nicotiana attenuata. Journal of Chemical Ecology 29, 763–770.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schjoerring JK,
Husted S,
Mack G, Mättsson M
(2002) The regulation of ammonium translocation in plants. Journal of Experimental Botany 53, 883–890.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smirnoff N, Stewart GR
(1985) Nitrate assimilation and translocation by higher plants: comparative physiology and ecological consequences. Physiologia Plantarum 64, 133–140.
Sperry JS, Hacke UG
(2004) Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes. American Journal of Botany 91, 369–385.
van der Schoot C, van Bel AJE
(1989) Architecture of the internodal xylem of tomato (Solanum lycopersicon) with reference to longitudinal and lateral transfer. American Journal of Botany 76, 487–503.
| Crossref |
Wanek W,
Arndt SK,
Huber W, Popp M
(2002) Nitrogen nutrition during ontogeny of hemiepiphytic Clusia species. Functional Plant Biology 29, 733–740.
| Crossref | GoogleScholarGoogle Scholar |
Watson MA, Casper BB
(1984) Morphogenetic constraints on patterns of carbon distribution in plants. Annual Review of Ecology and Systematics 15, 233–258.
| Crossref | GoogleScholarGoogle Scholar |
Zwieniecki MA,
Melcher PJ, Holbrook NM
(2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291, 1059–1062.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zwieniecki MA,
Orians CM,
Melcher PJ, Holbrook NM
(2003) Ionic control of the lateral exchange of water between vascular bundles in tomato. Journal of Experimental Botany 54, 1399–1405.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
