Damage to leaf veins suppresses root foraging precision.
Plantaginaceae
Rosaceae
long-distance signaling
plant behavior
root allocation
simulated herbivory
soil nutrient
Journal
American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467
Informations de publication
Date de publication:
08 2019
08 2019
Historique:
received:
12
03
2019
accepted:
04
06
2019
pubmed:
10
8
2019
medline:
23
2
2020
entrez:
10
8
2019
Statut:
ppublish
Résumé
Plants generally increase root growth in areas with high nutrients in heterogeneous soils, a phenomenon called foraging precision. The physiology of this process is not well understood, but it may involve shoot-root signaling via leaf veins. If this is true, then damage to leaf veins, but not to nearby mesophyll, would reduce plant foraging precision. To test this hypothesis, we imposed two leaf damage treatments on Plantago asiatica and Prunus jamasakura, removing either the tip of each main vein or mesophyll tissue between the veins with a 3-mm-diameter hole punch. After 30 days or 20 weeks of plant growth, we measured root biomass in the soil in response to soil nutrient concentration. When leaf mesophyll was damaged, root biomass of both species was greater in nutrient-rich patches than in nutrient-poor patches. However, when leaf veins were damaged, root biomass was similar between patches. These results suggest the importance of shoot-root signaling in plants, emphasizing that physiological processes are not necessarily restricted to single organs. The idea that herbivores that damage leaf veins may affect a plant's ability to selectively forage in high-nutrient patches is novel, with implications for natural and managed systems.
Substances chimiques
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1126-1130Subventions
Organisme : JSPS
ID : 18K19353
Pays : International
Organisme : JSPS
ID : 19H03295
Pays : International
Informations de copyright
© 2019 Botanical Society of America.
Références
Cahill, J. F., and G. G. McNickle. 2011. The behavioural ecology of nutrient foraging by plants. Annual Review of Ecology, Evolution, and Systematics 42: 289-311.
Chen, W., R. T. Koide, T. S. Adams, J. L. DeForest, L. Cheng, and D. M. Eissenstat. 2016. Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. Proceedings of the National Academy of Sciences, USA 113: 8741-8746.
Farley, R. A., and A. H. Fitter. 1999. Temporal and spatial variation in soil resources in a deciduous woodland. Journal of Ecology 87: 688-696.
Heil, M., B. Fiala, B. Baumann, and K. E. Linsenmair. 2000. Temporal, spatial and biotic variations in extrafloral nectar secretion by Macaranga tanarius. Functional Ecology 14: 749-757.
Hodge, A. 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162: 9-24.
Keeble, F., M. G. Nelson, and R. Snow. 1930. The integration of plant behaviour-II. The influence of the shoot on the growth of roots in seedlings. Proceedings of the Royal Society of London, B, Containing Papers of a Biological Nature 106: 182-188.
Ko, D., and Y. Helariutta. 2017. Shoot-root communications in flowering plants. Current Biology 27: 973-978.
O'Brien, E. E., M. Gersani, and J. S. Brown. 2005. Root proliferation and seed yield in response to spatial heterogeneity of below-ground competition. New Phytologist 168: 401-412.
Ohkubo, Y., M. Tanaka, R. Tabata, M. Ogawa-Ohnishi, and Y. Matsubayashi. 2017. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nature Plants 3: 17029.
Pulice, C. E., and A. A. Packer. 2008. Simulated herbivory induces extrafloral nectary production in Prunus avium. Functional Ecology 22: 801-807.
R Core Team. 2015. R. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Roth-Nebelsick, A., D. Uhl, V. Mosbrugger, and H. Kerp. 2001. Evolution and function of leaf venation architecture: a review. Annals of Botany 87: 553-566.
Ruffel, S., G. Krouk, D. Ristova, D. Shasha, K. D. Birnbaum, and G. M. Coruzzi. 2011. Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signalling for N supply vs. demand. Proceedings of the National Academy of Sciences, USA 108: 18524-18529.
Schoonhoven, L. M., J. J. A. van Loon, and M. Dick. 2012. Insect-plant biology, 2nd ed. Oxford University Press, Oxford, UK.
Snow, R., and M. A. Fellow. 1930. The influence of the shoot on the growth of roots in seedlings. The integration of Plant Behaviour II: 182-188.
Tabata, R., K. Sumida, T. Yoshii, K. Ohyama, H. Shinohara, and Y. Matsubayashi. 2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346: 343-346.
Takematsu T., and N. Ichizen. 1987. Weeds of the world, vol. 1, Sympetalae. Zenkoku Noson Kyoiku Kyokai, Tokyo, Japan.
Walters, D. R. 2011. Plant defense: warding off attack by pathogens, herbivores, and parasitic plants. Blackwell, Ames, IA, USA.
Wei, H., P. Guo, H. Zheng, X. He, P. Wang, Z. Ren, and C. Zhai. 2017. Micro-scale heterogeneity in urban forest soils affects fine root foraging by ornamental seedlings of Buddhist pine and northeast yew. Urban Forestry and Urban Greening 28: 63-72.
Wijesinghe, D. K., E. A. John, S. Beurskens, and M. J. Hutchings. 2004. Root system size and precision in nutrient foraging: response to spatial pattern of nutrient supply in six herbaceous species. Journal of Ecology 89: 972-983.
Yamawo, A., N. Suzuki, J. Tagawa, and Y. Hada. 2012. Leaf ageing promotes the shift in defence tactics in Mallotus japonicus from direct to indirect defence. Journal of Ecology 100: 802-809.