Abstract
Main conclusion
Nitrogen promotes changes in SLA through metabolism and anatomical traits in Capsicum plants.
Abstract
Specific leaf area (SLA) is a key trait influencing light interception and light use efficiency that often impacts plant growth and production. SLA is a key trait explaining growth variations of plant species under different environments. Both light and nitrogen (N) supply are important determinants of SLA. To better understand the effect of irradiance level and N on SLA in Capsicum chinense, we evaluated primary metabolites and morphological traits of two commercial cultivars (Biquinho and Habanero) in response to changes in both parameters. Both genotypes showed increased SLA with shading, and a decrease in SLA in response to increased N supply, however, with Habanero showing a stable SLA in the range of N deficiency to sufficient N doses. Correlation analyses indicated that decreased SLA in response to higher N supply was mediated by altered amino acids, protein, and starch levels, influencing leaf density. Moreover, in the range of moderate N deficiency to N sufficiency, both genotypes exhibited differences in SLA response, with Biquinho and Habanero displaying alterations on palisade and spongy parenchyma, respectively. Altogether, the results suggest that SLA responses to N supply are modulated by the balance between certain metabolites content and genotype-dependent changes in the parenchyma cells influencing leaf thickness and density.
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Abbreviations
- DAF:
-
Days after flowering
- LMA:
-
Leaf mass per area
- SLA:
-
Specific leaf area
References
An H, Shangguan Z-P (2008) Specific leaf area, leaf nitrogen content, and photosynthetic acclimation of Trifolium repens L. seedlings grown at different irradiances and nitrogen concentrations. Photosynthetica 46:143. https://doi.org/10.1007/s11099-008-0023-y
Barbosa JM, Singh NK, Cherry JH, Locy RD (2010) Nitrate uptake and utilization is modulated by exogenous γ-aminobutyric acid in Arabidopsis thaliana seedlings. Plant Physiol Biochem 48:443–450. https://doi.org/10.1016/j.plaphy.2010.01.020
Bosabalidis AM, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci 163:375–379. https://doi.org/10.1016/S0168-9452(02)00135-8
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Cavatte PC, Rodríguez-López NF, Martins SCV et al (2012) Functional analysis of the relative growth rate, chemical composition, construction and maintenance costs, and the payback time of Coffea arabica L. leaves in response to light and water availability. J Exp Bot 63:3071–3082. https://doi.org/10.1093/jxb/ers027
Chatterton NJ, Silvius JE (1981) Photosynthate partitioning into starch in soybean leaves: II. Irradiance level and daily photosynthetic period duration effects. Plant Physiol 67:257–260. https://doi.org/10.1104/pp.67.2.257
Cross JM, von Korff M, Altmann T et al (2006) Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiol 142:1574–1588. https://doi.org/10.1104/pp.106.086629
de Ávila Silva L, Condori-Apfata JA, de Costa PMA et al (2019a) Source strength modulates fruit set by starch turnover and export of both sucrose and amino acids in pepper. Plant Cell Physiol 60:2319–2330. https://doi.org/10.1093/pcp/pcz128
de Ávila Silva L, Condori-Apfata JA, Marcelino MM et al (2019b) Nitrogen differentially modulates photosynthesis, carbon allocation and yield related traits in two contrasting Capsicum chinense cultivars. Plant Sci 283:224–237. https://doi.org/10.1016/j.plantsci.2019.02.014
Dijkstra P, Lambers H (1989) Analysis of specific leaf area and photosynthesis of two inbred lines of Plantago major differing in relative growth rate. New Phytol 113:283–290. https://doi.org/10.1111/j.1469-8137.1989.tb02405.x
Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2001) Fructose 2,6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling heterotrophic cells. Planta 212:250–263. https://doi.org/10.1007/s004250000386
Garnier E, Laurent G (1994) Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytol. https://doi.org/10.1111/j.1469-8137.1994.tb04036.x
Garnier E, Cordonnier P, Guillerm J, Sonié L (1997) Specific leaf area and leaf nitrogen concentration in annual and perennial grass species growing in Mediterranean old-fields. Oecologia 111:490–498. https://doi.org/10.1007/s004420050262
Gratani L, Covone F, W L (2006) Leaf plasticity in response to light of three evergreen species of the Mediterranean maquis. Trees 20:549–558. https://doi.org/10.1007/s00468-006-0070-6
Hanba YT, Miyazawa S-I, Terashima I (1999) The influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests. Funct Ecol 13:632–639. https://doi.org/10.1046/j.1365-2435.1999.00364.x
Jing Y, Cui D, Bao F et al (2009) Tryptophan deficiency affects organ growth by retarding cell expansion in Arabidopsis. Plant J 3:511–521. https://doi.org/10.1111/j.1365-313X.2008.03706.x
Jinwen L, Jingping Y, Pinpin F et al (2009) Responses of rice leaf thickness, SPAD readings and chlorophyll a/b ratios to different nitrogen supply rates in paddy field. F Crop Res 114:426–432. https://doi.org/10.1016/j.fcr.2009.09.009
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Co., Inc., New York, NY
Kalra PY (1998) Handbook of reference methods for plant analysis. Crop Sci 38:1710. https://doi.org/10.2135/cropsci1998.0011183X003800060050x
Knops JMH, Reinhart K (2000) Specific leaf area along a nitrogen fertilization gradient. Am Midl Nat 144:265–272. https://doi.org/10.1674/0003-0031(2000)144[0265:SLAAAN]2.0.CO;2
LeBel P, Bradley RL, Thiffault N (2013) The relative importance of nitrogen vs. moisture stress may drive intraspecific variations in the SLA-RGR relationship: the case of Picea mariana seedlings. Sci Rep 4:1278–1284. https://doi.org/10.4236/ajps.2013.46158
Liu M, Wang Z, Li S et al (2017) Changes in specific leaf area of dominant plants in temperate grasslands along a 2500 km transect in northern China. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-11133-z
Lloyd J, Syvertsen JP, Kriedemann PE, Farquhar GD (1992) Low conductances for CO2 diffusion from stomata to the sites of carboxylation in leaves of woody species. Plant Cell Environ 15:873–899. https://doi.org/10.1111/j.1365-3040.1992.tb01021.x
McDonald AJS, Lohammar T, Ericsson A (1986) Growth response to step-decrease in nutrient availability in small birch (Betula pendula Roth). Plant Cell Environ 9:427–432. https://doi.org/10.1111/j.1365-3040.1986.tb01756.x
Medina-Lara F, Echevarría-Machado I, Pacheco-Arjona R et al (2008) Influence of nitrogen and potassium fertilization on fruiting and capsaicin content in habanero pepper (Capsicum chinense Jacq.). HortScience 43:1549–1554. https://doi.org/10.1017/CBO9781107415324.004
Meziane D, Shipley B (1999) Interacting determinants of specific leaf area in 22 herbaceous species: effects of irradiance and nutrient availability. Plant Cell Environ 22:447–459. https://doi.org/10.1046/j.1365-3040.1999.00423.x
Mooney HA, Ferrar PJ, Slatyer RO (1978) Photosynthetic capacity and carbon allocation patterns in diverse growth forms of Eucalyptus. Oecologia 36:103–111. https://doi.org/10.1007/BF00344575
Niinemets Ü (1997) Distribution patterns of foliar carbon and nitrogen as affected by tree dimensions and relative light conditions in the canopy of Picea abies. Trees 11:144–154. https://doi.org/10.1007/PL00009663
Novais RF, Neves JCL, Barros NF (1991) Ensaio em ambiente controlado. EMBRAPA, Brasília DF
Nunes-Nesi A, Carrari F, Gibon Y et al (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J 50:1093–1106. https://doi.org/10.1111/j.1365-313X.2007.03115.x
O’Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termarcarphi, Melbourne, Australia
Olsen JK, Lyons PJ, Kelly MM (1993) Nitrogen uptake and ultiization by Bell Pepper in subtropical Australia. J Plant Nutr 16:177–193. https://doi.org/10.1080/01904169309364521
Padgett PE, Leonard RT (1996) Free amino acid levels and the regulation of nitrate uptake in maize cell suspension cultures. J Exp Bot 47:871–883. https://doi.org/10.1093/jxb/47.7.871
Pompelli M, Martins S, Celin E et al (2010) What is the influence of ordinary epidermal cells and stomata on the leaf plasticity of coffee plants grown under full-sun and shady conditions? Brazilian J Biol 70:1083–1088. https://doi.org/10.1590/S1519-69842010000500025
Poorter H, Pothmann P (1992) Growth and carbon economy of a fast-growing and a slow-growing grass species as dependent on ontogeny. New Phytol 120:159–166. https://doi.org/10.1111/j.1469-8137.1992.tb01069.x
Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83:553–559. https://doi.org/10.1007/BF00317209
Poorter H, Villar R (1997) The fate of acquired carbon in plants: Chemical composition and construction costs. In: Bazzaz FA, Grace JBT (eds) Plant resource allocation. Academic Press, San Diego, pp 39–72
Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol 94:621–627. https://doi.org/10.1104/pp.94.2.621
Poorter H, Niinemets Ü, Poorter L et al (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588. https://doi.org/10.1111/j.1469-8137.2009.02830.x
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta: Bioenerg 975:384–394. https://doi.org/10.1016/S0005-2728(89)80347-0
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Reich PB, Walters MB (1994) Photosynthesis-nitrogen relations in Amazonian tree species. II. Variation in nitrogen vis-a-vis specific leaf area influences mass- and area-based expressions. Oecologia 97:73–81. https://doi.org/10.1007/BF00317910
Reich PB, Walters MB, Ellsworth DS, Uhl C (1994) Photosynthesis-nitrogen relations in Amazonian tree species. I Patterns among species and communities. Oecologia 97:62–72. https://doi.org/10.1007/BF00317909
Reich PB, Ellsworth DS, Walters MB (1998) Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Funct Ecol 12:948–958. https://doi.org/10.1046/j.1365-2435.1998.00274.x
Rufty TW, Huber SC, Volk RJ (1988) Alterations in leaf carbohydrate metabolism in response to nitrogen stress. Plant Physiol 88:725–730. https://doi.org/10.1104/pp.88.3.725
Sarasketa A, González-Moro MB, González-Murua C, Marino D (2014) Exploring ammonium tolerance in a large panel of Arabidopsis thaliana natural accessions. J Exp Bot 65:6023–6033. https://doi.org/10.1093/jxb/eru342
Scheible WR, Gonzalez-Fontes A, Lauerer M et al (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798. https://doi.org/10.1105/tpc.9.5.783
Shipley B (1995) Structured interspecific determinants of specific leaf area in 34 species of herbaceous angiosperms. Br Ecol Soc 9:312–319. https://doi.org/10.2307/2390579
Shipley B (2000) Plasticity in relative growth rate and its components following a change in irradiance. Plant Cell Environ 23:1207–1216. https://doi.org/10.1046/j.1365-3040.2000.00635.x
Shipley B, Almeida-Cortez J (2003) Interspecific consistency and intraspecific variability of specific leaf area with respect to irradiance and nutrient availability Interspecific consistency and intraspecific variability of specific leaf area with respect to irradiance and. Écoscience 10(1):74–79. https://doi.org/10.1080/11956860.2003.11682753
Shvaleva AL, Silva FCE, Breia E et al (2006) Metabolic responses to water deficit in two Eucalyptus globulus clones with contrasting drought sensitivity. Tree Physiol 25:239–248. https://doi.org/10.1093/treephys/26.2.239
Sienkiewicz-Porzucek A, Sulpice R, Osorio S et al (2010) Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Mol Plant 3:156–173. https://doi.org/10.1093/mp/ssp101
Steel RGD, Torrie JH, Dickey DA (1997) Principles and procedures of statistics: a biometrical approach, 3rd edn. McGraw-Hill, New York
Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2:178–186. https://doi.org/10.1016/S1369-5266(99)80033-8
Terashima I, Hikosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant Cell Environ 18:1111–1128. https://doi.org/10.1111/j.1365-3040.1995.tb00623.x
Tian M, Yu G, He N, Hou J (2016) Leaf morphological and anatomical traits from tropical to temperate coniferous forests: mechanisms and influencing factors. Sci Rep. https://doi.org/10.1038/srep19703
Van Arendonk JJCM, Poorter H (1994) The chemical composition and anatomical structure of leaves of grass species differing in relative growth rate. Plant Cell Environ 17:963–970. https://doi.org/10.1111/j.1365-3040.1994.tb00325.x
Van Arendonk JJCM, Niemann GJ, Boon JJ, Lambers H (1997) Effects of nitrogen supply on the anatomy and chemical composition of leaves of four grass species belonging to the genus Poa, as determined by image-processing analysis and pyrolysis–mass spectrometry. Plant Cell Environ 20:881–897. https://doi.org/10.1046/j.1365-3040.1997.d01-135.x
Van Den Boogaard R, Alewijnse D, Veneklaas EJ, Lambers H (1997) Growth and water-use efficiency of 10 Triticum aestivum cultivars at different water availability in relation to allocation of biomass. Plant Cell Environ 20:200–210. https://doi.org/10.1046/j.1365-3040.1997.d01-60.x
Wany A, Foyer CH, Gupta KJ (2018) Nitrate, NO and ROS signaling in stem cell homeostasis. Trends Plant Sci 23:1041–1044. https://doi.org/10.1016/j.tplants.2018.09.010
Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88:486–493. https://doi.org/10.1007/BF00317710
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Xiong D, Wang D, Liu X et al (2016) Leaf density explains variation in leaf mass per area in rice between cultivars and nitrogen treatments. Ann Bot 117:963–971. https://doi.org/10.1093/aob/mcw022
Acknowledgements
Financial support was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (grant number 306818/2016-7 to ANN, 501090/2015-0 to LAS, and RS, 402511/2016-6 to WLA). Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) [grant number: CRA-RED-00053-16 to ANN]. Research fellowships granted by CNPq to RPO-G (process number 152121/2019-6), ANN, FMD, and WLA are also gratefully acknowledged. RS was supported by a Research Stimulus Grant (VICCI—Grant No: 14/S/819) funded the Irish Department of Agriculture, Food and the Marine (DAFM). We also thank Ms. Franciele Santos Oliveira for the support with the sample’s preparation.
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de Ávila Silva, L., Omena-Garcia, R.P., Condori-Apfata, J.A. et al. Specific leaf area is modulated by nitrogen via changes in primary metabolism and parenchymal thickness in pepper. Planta 253, 16 (2021). https://doi.org/10.1007/s00425-020-03519-7
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DOI: https://doi.org/10.1007/s00425-020-03519-7