Leaf green-white variegation is advantageous under N deprivation in Pelargonium × hortorum
Cyril Abadie A , Marlène Lamothe B , Caroline Mauve B , Françoise Gilard B and Guillaume Tcherkez A C D E
+ Author Affiliations
- Author Affiliations
A Institut de Biologie des Plantes, CNRS UMR 8618, Université Paris-Sud, 91405 Orsay cedex, France.
B Plateforme Métabolisme-Métabolome, Université Paris-Sud, 91405 Orsay cedex, France.
C Institut Universitaire de France, 103 boulevard Saint-Michel, 75005 Paris, France.
D Present address: Research School of Biology, ANU College of Medicine, Biology and Environment, Australian National University, Canberra, ACT 2601, Australia.
E Corresponding author. Email: guillaume.tcherkez@u-psud.fr
Functional Plant Biology 42(6) 543-551 https://doi.org/10.1071/FP14250
Submitted: 15 September 2014 Accepted: 9 February 2015 Published: 17 March 2015
Abstract
Variegation (patchy surface area with different colours) is a common trait of plant leaves. In green-white variegated leaves, two tissues with contrasted primary carbon metabolisms (autotrophic in green and heterotrophic in white tissues) are juxtaposed. It is generally believed that variegation is detrimental to growth due to the lower photosynthetic surface area. However, the common occurrence of leaf variegation in nature raises the question of a possible advantage under certain circumstances. Here, we examined growth and metabolism of variegated Pelargonium × hortorum L.H.Bailey using metabolomics techniques under N deprivation. Our results showed that variegated plants tolerate N deficiency much better, i.e. do not stop leaf biomass production after 9 weeks of N deprivation, even though the growth of green plants is eventually arrested and leaf senescence is triggered. Metabolic analysis indicates that white areas are naturally enriched in arginine, which decreases a lot upon N deprivation, probably to feed green areas. This process may compensate for the lower proteolysis enhancement in green areas and thus contribute to maintaining photosynthetic activity. We conclude that under our experimental conditions, leaf variegation was advantageous under prolonged N deprivation.
Additional keywords: arginine, metabolomics, N deficiency, remobilization.
References
Aluru MR, Zola J, Foudree A, Rodermel SR (2009) Chloroplast photooxidation-induced transcriptome reprogramming in Arabidopsis immutans white leaf sectors. Plant Physiology 150, 904–923.| Chloroplast photooxidation-induced transcriptome reprogramming in Arabidopsis immutans white leaf sectors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsleitbg%3D&md5=3c29c16954c180f4940b24bba53215cbCAS | 19386811PubMed |
Amberger-Ochsenbauer S, Taylor M, Lohr D, Meinken E (2010) Effect of increasing ratios of urea-N in the nutrient solution on growth of Pelargonium (Pelargonium × hortorum). Acta Horticulturae 938, 243–250.
Batagelj V, Mrvar A (2004) ‘Pajek - analysis and visualization of large networks. Graph drawing software.’ pp. 77–103. (Springer: Berlin)
Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communications in Soil Science and Plant Analysis 6, 71–80.
| Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhs1Kqt7Y%3D&md5=ce227ec5c90d6c80eb18a9193e19b097CAS |
Cruz JL, Mosquim PR, Pelacani CR, Araujo WL, DaMata FM (2003) Photosynthesis impairment in cassava leaves in response to nitrogen deficiency. Plant and Soil 257, 417–423.
| Photosynthesis impairment in cassava leaves in response to nitrogen deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXoslWrt7g%3D&md5=1946650a62354ef1b9ccdfc9048caa3aCAS |
DeKock PC, Morrison RI (1958) The metabolism of chlorotic leaves. 1. Amino acids. Bioch 70, 266–272.
Downton WJS, Grant WJR (1994) Photosynthetic and growth responses of variegated ornamental species to elevated CO2. Australian Journal of Plant Physiology 21, 273–279.
| Photosynthetic and growth responses of variegated ornamental species to elevated CO2.Crossref | GoogleScholarGoogle Scholar |
Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the United States of America 95, 14863–14868.
| Cluster analysis and display of genome-wide expression patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVGmurk%3D&md5=25f1bb3e4037791e89610e1da4366f1bCAS | 9843981PubMed |
Evenari M (1989) The history of research on white-green variegated plants. Botanical Review 55, 106–139.
| The history of research on white-green variegated plants.Crossref | GoogleScholarGoogle Scholar |
Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. Journal of Experimental Botany 59, 1615–1624.
| Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlelt7c%3D&md5=3e1bb23a99d8db234803d86fbfcef110CAS | 17975207PubMed |
Gaufichon L, Masclaux-Daubresse C, Tcherkez G, Reisdorf-Cren M, Sakakibara Y, Hase T, Clément G, Avice JC, Granjean O, Marmagne A, Boutet-Mercey S, Azzopardi M, Soulay F, Suzuki A (2013) Arabidopsis thaliana Asn2 encoding asparagine synthetase is involved in the control of nitrogen assimilation and export during vegetative growth. Plant, Cell & Environment 36, 328–342.
| Arabidopsis thaliana Asn2 encoding asparagine synthetase is involved in the control of nitrogen assimilation and export during vegetative growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjslWhtw%3D%3D&md5=35252137e1b01d525d4f4f39380f1eadCAS |
Givnish TJ (1990) Leaf mottling: relation to growth form and leaf phenology and possible role as camouflage. Functional Ecology 4, 463–474.
| Leaf mottling: relation to growth form and leaf phenology and possible role as camouflage.Crossref | GoogleScholarGoogle Scholar |
Godel H, Graser T, Földi P, Pfaender P, Fürst P (1984) Measurement of free amino acids in human biological fluids by high-performance liquid chromatography. Journal of Chromatography. A 297, 49–61.
| Measurement of free amino acids in human biological fluids by high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXltVKktro%3D&md5=a97dacc164b18fb94e0e322a7e04cb80CAS |
Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany 53, 927–937.
| Nitrogen metabolism and remobilization during senescence.Crossref | GoogleScholarGoogle Scholar | 11912235PubMed |
Ivanova TI, Sherstneva OA (1999) Dark respiration of variegated leaves in plants of different life forms. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 46, 666–673.
Jia Y, Gray VM (2003) Interrelationships between nitrogen supply and photosynthetic parameters in Vicia faba L. Photosynthetica 41, 605–610.
| Interrelationships between nitrogen supply and photosynthetic parameters in Vicia faba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVKnsr8%3D&md5=807075600e94621af78fa7aad59b08f6CAS |
Jones H, Eagles JE (1962) Translocation of 14C-carbon within and between leaves. Annals of Botany 26, 505–510.
Lea US, Slimestad R, Smevig P, Lillo C (2007) Nitrogen deficiency enhances expression of specific MYB and bHLH transcripts and accumulation of end products in the flavonoid pathway. Planta 225, 1245–1253.
| Nitrogen deficiency enhances expression of specific MYB and bHLH transcripts and accumulation of end products in the flavonoid pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtVWjs7o%3D&md5=9a46a6a3c2e4790dd39d6f1c764f8c8eCAS | 17053893PubMed |
Madore MA (1990) Carbohydrate metabolism in photosynthetic and non-photosynthetic tissues of variegated leaves of Coleus blumei Benth. Plant Physiology 93, 617–622.
| Carbohydrate metabolism in photosynthetic and non-photosynthetic tissues of variegated leaves of Coleus blumei Benth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslCqurY%3D&md5=0c87ce962c09421205b5bb7c604d988fCAS | 16667512PubMed |
Masclaux C, Quilleré I, Gallais A, Hirel B (2001) The challenge of remobilisation in plant nitrogen economy. A survey of physio-agronomic and molecular approaches. Annals of Applied Biology 138, 69–81.
| The challenge of remobilisation in plant nitrogen economy. A survey of physio-agronomic and molecular approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvVOmt7k%3D&md5=0a27adeda9953f702774dd7aaa858915CAS |
Masclaux-Daubresse C, Chardon F (2011) Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. Journal of Experimental Botany 62, 2131–2142.
| Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsFyjtbo%3D&md5=a1167ff5cb371a58ce4b1c614036ae1fCAS | 21273332PubMed |
Pringsheim EG, Schwarz W (1933) Das Auftretenweissbunter(panaschierter) Pflanzen in der Natur. Flora 28, 111–122.
Rosso D, Bode R, Li W, Krol M, Saccon D, Wang S, Schillaci LA, Rodermel SR, Maxwell DP, Hüner NPA (2009) Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1 and var2. The Plant Cell 21, 3473–3492.
| Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1 and var2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWrtQ%3D%3D&md5=4afa61ec56ae839ee057aadaefa48500CAS | 19897671PubMed |
Seemann JR, Sharkey TD (1986) Saminity and nitrogen effects on photosynthesis, ribulose-1,5-bisphosphate carboxylase and metabolite pool sizes in Phaseolus vulgaris. Plant Physiology 82, 555–560.
| Saminity and nitrogen effects on photosynthesis, ribulose-1,5-bisphosphate carboxylase and metabolite pool sizes in Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XmtVKnsLc%3D&md5=8869b5c5ad50ac4ccb76db6d0c5a7ccdCAS | 16665066PubMed |
Seltmann H (1955) Comparative physiology of green and albino corn seedlings. Plant Physiology 30, 258–263.
| Comparative physiology of green and albino corn seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2MXosFWguw%3D%3D&md5=01d0e648c330856bf0d00c97ce653946CAS | 16654766PubMed |
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
| Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiur3F&md5=82578db68694d79cb87c996f505523e8CAS |
Smith AP (1986) Ecology of a leaf color polymorphism in a tropical forest species: habitat segregation and herbivory. Oecologia 69, 283–287.
| Ecology of a leaf color polymorphism in a tropical forest species: habitat segregation and herbivory.Crossref | GoogleScholarGoogle Scholar |
Tcherkez G, Mahé A, Gauthier P, Mauve C, Gout E, Bligny R, Cornic G, Hodges M (2009) In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D isotope effects highlight the non-cyclic nature of the tricarboxylic acid “cycle’’ in illuminated leaves. Plant Physiology 151, 620–630.
| In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D isotope effects highlight the non-cyclic nature of the tricarboxylic acid “cycle’’ in illuminated leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12qu7fK&md5=afc9835be4ebe96ff4b5032ce245c292CAS | 19675152PubMed |
Tcherkez G, Guérard F, Gilard F, Lamothe M, Mauve C, Gout E, Bligny R (2012) Metabolomic characterization of the functional division of nitrogen metabolism in variegated leaves. Functional Plant Biology 39, 959–967.
| Metabolomic characterization of the functional division of nitrogen metabolism in variegated leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKru7%2FN&md5=2bbdd5ff79ad57294135982aa78779d7CAS |
Toshoji H, Katsumata T, Takusagawa M, Yusa Y, Sakai A (2012) Effects of chloroplast dysfunction on mitochondria: white sectors in variegated leaves have higher mitochondrial DNA levels and lower dark respiration rates than green sectors. Protoplasma 249, 805–817.
| Effects of chloroplast dysfunction on mitochondria: white sectors in variegated leaves have higher mitochondrial DNA levels and lower dark respiration rates than green sectors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xpt1yjsLg%3D&md5=c2dd3a6b450393b0b58170693c1b0937CAS | 21984314PubMed |
Urbanczyk-Wochniak E, Fernie AR (2005) Metabolic profiling reveals altered nitrogen nutrient regimes have diverse effects on the metabolism of hydroponically-grown tomato (Solanum lycopersicum) plants. Journal of Experimental Botany 56, 309–321.
| Metabolic profiling reveals altered nitrogen nutrient regimes have diverse effects on the metabolism of hydroponically-grown tomato (Solanum lycopersicum) plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1WltQ%3D%3D&md5=ff521f52a9b9b8f31006fa7862dc5163CAS | 15596475PubMed |
Vaughn KC, Stewart KD (1978) Light-harvesting pigment-protein complex deficiency in Hosta (Liliaceae). Planta 143, 275–278.
| Light-harvesting pigment-protein complex deficiency in Hosta (Liliaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXjs1Cgtw%3D%3D&md5=6a3d8278c3c321703890f549495210deCAS | 24408465PubMed |
Witte CP (2011) Urea metabolism in plants. Plant Science 180, 431–438.
| Urea metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvFSitw%3D%3D&md5=4c07902e29de4d6725f62108421d29b7CAS | 21421389PubMed |
