, Volume 242, Issue 3, pp 677–691 | Cite as

Exploring natural variation of photosynthetic, primary metabolism and growth parameters in a large panel of Capsicum chinense accessions

  • Laise Rosado-Souza
  • Federico Scossa
  • Izabel S. Chaves
  • Sabrina Kleessen
  • Luiz F. D. Salvador
  • Jocimar C. Milagre
  • Fernando Finger
  • Leonardo L. Bhering
  • Ronan Sulpice
  • Wagner L. Araújo
  • Zoran Nikoloski
  • Alisdair R. Fernie
  • Adriano Nunes-NesiEmail author
Original Article


Main conclusion

Collectively, the results presented improve upon the utility of an important genetic resource and attest to a complex genetic basis for differences in both leaf metabolism and fruit morphology between natural populations.

Diversity of accessions within the same species provides an alternative method to identify physiological and metabolic traits that have large effects on growth regulation, biomass and fruit production. Here, we investigated physiological and metabolic traits as well as parameters related to plant growth and fruit production of 49 phenotypically diverse pepper accessions of Capsicum chinense grown ex situ under controlled conditions. Although single-trait analysis identified up to seven distinct groups of accessions, working with the whole data set by multivariate analyses allowed the separation of the 49 accessions in three clusters. Using all 23 measured parameters and data from the geographic origin for these accessions, positive correlations between the combined phenotypes and geographic origin were observed, supporting a robust pattern of isolation-by-distance. In addition, we found that fruit set was positively correlated with photosynthesis-related parameters, which, however, do not explain alone the differences in accession susceptibility to fruit abortion. Our results demonstrated that, although the accessions belong to the same species, they exhibit considerable natural intraspecific variation with respect to physiological and metabolic parameters, presenting diverse adaptation mechanisms and being a highly interesting source of information for plant breeders. This study also represents the first study combining photosynthetic, primary metabolism and growth parameters for Capsicum to date.


Capsicum Natural genetic variation Pepper Photosynthesis Primary metabolism Respiration 



Actual quantum yield of PSII electron transport


Dark respiration


Dry weight


Intrinsic water use efficiency


Maximum photochemical efficiency of PSII


Net carbon assimilation


Non-photochemical quenching


Photochemical quenching


Relative growth rate


Specific leaf area


Stomatal conductance


Transpiration rates



This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [grant number 306355/2012-4 and 484675/2013-3 to ANN and 472787/2011-0 to WLA], Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) [grant numbers APQ-01713-13 and APQ-02548-13] and Max Planck Society to ANN and WLA. Research fellowships granted by CNPq to ANN and WLA are also gratefully acknowledged. The authors also acknowledge the NUBIOMOL-UFV for providing the facilities for the analysis of this work. Thanks are also due to Jéssica Maciel Terra and Franklin Magnum de Oliveira Silva (UFV) for help in the experiments and statistical analysis.

Supplementary material

425_2015_2332_MOESM1_ESM.pdf (198 kb)
Supplementary Table S1 Origin and location from 49 C. chinense accessions. Horticultural germplasm bank files at Federal University of Viçosa (UFV). Supplementary Table S2 Profiles of the biochemical components, including sugars (fructose, glucose and sucrose), starch, organic acids (malate and fumarate), nitrate, total amino acids, total protein, chlorophyll a and b, as well as growth-related parameters for the 49 accessions grown in the second experiment. Samples for metabolites measurements were harvested at the middle of the light period. Values are presented as mean ± SE (n = 4). Different letters represent the groups formed by Modified Scott-Knot test (P ≤ 0.05). Abbreviations: RGR, relative growth rate; DW, dry weight; F v /F m , maximum photochemical efficiency of photosystem II; Φ PSII, actual quantum yield of photosystem II electron transport; qP, photochemical quenching coefficient; NPQ, non-photochemical quenching. Supplementary Table S3 Geographic variability analysis of biochemical and growth-related profiles. Moran’s I, Geary’s C and Global G statistics are calculated for two different experiments separately and combined. The statistics are based on gathered biochemical profiles from 49 C. chinense accessions (PDF 197 kb)
425_2015_2332_MOESM2_ESM.pdf (204 kb)
Supplementary Fig. S1 Dendogram obtained from growth parameters (SLA, RGR, Shoot DW and plant height) data set by the Mahalanobis distance measure and cluster analysis by unweighte pair-group method of arithmetic averages (UPGMA) (Mojena 1977) of 49 C. chinense accessions. Dashed red line corresponds to the cut statistically significant in the similarity axis. Abbreviations: Accession (a), Cluster 1 (C1), Cluster 2 (C2) and Cluster 3 (C3). Supplementary Fig. S2 Gas exchange parameters and chlorophyll a fluorescence parameters of 49 C. chinense accessions. Intrinsic water use efficiency (WUE) (a); transpiration rates (E) (b); dark respiration (R d ) (c); maximum photochemical efficiency of photosystem II (F v /F m ) (d); photochemical quenching coefficient (qP) (e); non-photochemical quenching (NPQ) (f). Values are presented as mean ± SE (n = 4). Different letters and colors represent the groups formed by Modified Scott-Knot test (P ≤ 0.05). Supplementary Fig. S3 Dendogram obtained from physiological parameters (stomatal density, A, g s , WUE, Ci, F v /F m , qP, NPQ, Φ PSII, E and Rd) data set by the Mahalanobis distance measure and cluster analysis by unweighte pair-group method of arithmetic averages (UPGMA) (Mojena 1977) of 49 C. chinense accessions. Dashed red line corresponds to the cut statistically significant in the similarity axis. Abbreviations: Accession (a), Cluster 1 (C1), Cluster 2 (C2) and Cluster 3 (C3). Supplementary Fig. S4 Nitrogen containing compounds in leaves of 49 C. chinense accessions. Chlorophyll a (Chl a) (a); chlorophyll b (Chl b) (b); chlorophyll a/b ratio (Chl a/b ratio) (c); nitrate (NO3) (d); total amino acids (e); total protein (f). Values are presented as mean ± SE (n = 4). Different letters and colors represent the groups formed by Modified Scott-Knot test (P ≤ 0.05). Supplementary Fig. S5 Carbon containing compounds in leaves of plants from 49 C. chinense accessions, harvested at the middle of the light period. Glucose (a); fructose (b); sucrose (c); starch (d); malate (e); fumarate (f). Values are presented as mean ± SE (n = 4). Different letters and colors represent the groups formed by Modified Scott-Knot test (P ≤ 0.05). Supplementary Fig. S6 Dendogram obtained from profile of metabolites (Chl a, Chl b, glucose, fructose, sucrose, starch, malate, fumarate, nitrate, amino acids and total protein) data set by the Mahalanobis distance measure and cluster analysis by unweighted pair-group method of arithmetic averages (UPGMA) (Mojena 1977) of 49 C. chinense accessions. Dashed red line corresponds to the cut statistically significant in the similarity axis. Abbreviations: Accession (a) (PDF 203 kb)


  1. Aloni B, Karni L, Zaidman Z, Schaffer AA (1996) Changes of carbohydrates in pepper (Capsicum annuum L) flowers in relation to their abscission under different shading regimes. Ann Bot 78:163–168CrossRefGoogle Scholar
  2. Araújo WL, Nunes-Nesi A, Fernie AR (2011a) Fumarate: multiple functions of a simple metabolite. Phytochemistry 72:838–843CrossRefPubMedGoogle Scholar
  3. Araújo WL, Nunes-Nesi A, Osorio S, Usadel B, Fuentes D, Nagy R, Balbo I, Lehmann M, Studart-Witkowski C, Tohge T, Martinoia E, Jordana X, Damatta FM, Fernie AR (2011b) Antisense inhibition of the iron-sulphur subunit of succinate dehydrogenase enhances photosynthesis and growth in tomato via an organic acid-mediated effect on stomatal aperture. Plant Cell 23:600–627PubMedCentralCrossRefPubMedGoogle Scholar
  4. Aza-Gonzalez C, Nunez-Palenius HG, Ochoa-Alejo N (2011) Molecular biology of capsaicinoid biosynthesis in chili pepper (Capsicum spp.). Plant Cell Rep 30:695–706CrossRefPubMedGoogle Scholar
  5. Bhering LL, Cruz CD, de Vasconcelos ES, Ferreira A, de Resende MFR Jr (2008) Alternative methodology for Scott-Knott test. Crop Breed Appl Biotechnol 8:9–16CrossRefGoogle Scholar
  6. Brand A, Borovsky Y, Meir S, Rogachev I, Aharoni A, Paran I (2012) pc8.1, a major QTL for pigment content in pepper fruit, is associated with variation in plastid compartment size. Planta 235:579–588CrossRefPubMedGoogle Scholar
  7. Cavatte PC, Oliveira AA, Morais LE, Martins SC, Sanglard LM, DaMatta FM (2012) Could shading reduce the negative impacts of drought on coffee? A morphophysiological analysis. Physiol Plant 144:111–122CrossRefPubMedGoogle Scholar
  8. Centeno DC, Osorio S, Nunes-Nesi A, Bertolo AL, Carneiro RT, Araujo WL, Steinhauser MC, Michalska J, Rohrmann J, Geigenberger P, Oliver SN, Stitt M, Carrari F, Rose JK, Fernie AR (2011) Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. Plant Cell 23:162–184PubMedCentralCrossRefPubMedGoogle Scholar
  9. Chaim AB, Paran I, Grube RC, Jahn M, van Wijk R, Peleman J (2001) QTL mapping of fruit-related traits in pepper (Capsicum annuum). Theor Appl Genet 102:1016–1028CrossRefGoogle Scholar
  10. Cross JM, von Korff M, Altmann T, Bartzetko L, Sulpice R, Gibon Y, Palacios N, Stitt M (2006) Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiol 142:1574–1588PubMedCentralCrossRefPubMedGoogle Scholar
  11. Cruz CD (2013) GENES—a software package for analysis in experimental statistics and quantitative genetics. Acta Scientiarum Agron 35:271–276Google Scholar
  12. DaMatta FM, Loos RA, Rodrigues R, Barros RS (2001) Actual and potential photosynthetic rates of tropical crop species. Brazil J Plant Physiol 13:24–32Google Scholar
  13. Driever SM, Lawson T, Andralojc PJ, Raines CA, Parry MA (2014) Natural variation in photosynthetic capacity, growth, and yield in 64 field-grown wheat genotypes. J Exp Bot 65:4959–4973PubMedCentralCrossRefPubMedGoogle Scholar
  14. El-Lithy ME, Rodrigues GC, van Rensen JJS, Snel JFH, Dassen H, Koornneef M, Jansen MAK, Aarts MGM, Vreugdenhil D (2005) Altered photosynthetic performance of a natural Arabidopsis accession is associated with atrazine resistance. J Exp Bot 56:1625–1634CrossRefPubMedGoogle Scholar
  15. Farquhar GD, von Caemmerer S, Berry JA (2001) Models of photosynthesis. Plant Physiol 125:42–45PubMedCentralCrossRefPubMedGoogle Scholar
  16. Fernie AR, Martinoia E (2009) Malate. Jack of all trades or master of a few? Phytochemistry 70:828–832CrossRefPubMedGoogle Scholar
  17. Fernie AR, Roessner U, Trethewey RN, Willmitzer L (2001) The contribution of plastidial phosphoglucomutase to the control of starch synthesis within the potato tuber. Planta 213:418–426CrossRefPubMedGoogle Scholar
  18. Finger FL, Lannes SD, Schuelter AR, Doege J, Comerlato AP, Goncalves LS, Ferreira FR, Clovis LR, Scapim CA (2010) Genetic diversity of Capsicum chinensise (Solanaceae) accessions based on molecular markers and morphological and agronomic traits. Genet Mol Res 9:1852–1864CrossRefPubMedGoogle Scholar
  19. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Hohne M, Hendriks JH, Palacios N, Cross J, Selbig J, Stitt M (2004) A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16:3304–3325PubMedCentralCrossRefPubMedGoogle Scholar
  20. Hair JF, Anderson TE, Tatham RL, Black WC (1998) Multivariate data analysis, 5th edn. Prentice Hall 1, Upper Saddle River, NJGoogle Scholar
  21. Hu C, Shi J, Quan S, Cui B, Kleessen S, Nikoloski Z, Tohge T, Alexander D, Guo L, Lin H, Wang J, Cui X, Rao J, Luo Q, Zhao X, Fernie AR, Zhang D (2014) Metabolic variation between japonica and indica rice cultivars as revealed by non-targeted metabolomics. Sci Rep 4:5067PubMedGoogle Scholar
  22. Ince AG, Karaca M, Onus AN (2009) Development and utilization of diagnostic DAMD-PCR markers for Capsicum accessions. Genet Resour Crop Evol 56:211–221CrossRefGoogle Scholar
  23. Kang M, Yang L, Zhang B, de Reffye P (2011) Correlation between dynamic tomato fruit-set and source–sink ratio: a common relationship for different plant densities and seasons? Ann Bot 107:805–815PubMedCentralCrossRefPubMedGoogle Scholar
  24. Keurentjes JJ, Sulpice R (2009) The role of natural variation in dissecting genetic regulation of primary metabolism. Plant Signal Behav 4:244–246PubMedCentralCrossRefPubMedGoogle Scholar
  25. Kleessen S, Antonio C, Sulpice R, Laitinen R, Fernie AR, Stitt M, Nikoloski Z (2012) Structured patterns in geographic variability of metabolic phenotypes in Arabidopsis thaliana. Nat Commun 3:1319CrossRefPubMedGoogle Scholar
  26. Kleessen S, Klie S, Nikoloski Z (2013) Data integration through proximity-based networks provides biological principles of organization across scales. Plant Cell 25:1917–1927PubMedCentralCrossRefPubMedGoogle Scholar
  27. Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172CrossRefPubMedGoogle Scholar
  28. Lannes SD, Finger FL, Schuelter AR, Casali VWD (2007) Growth and quality of Brazilian accessions of Capsicum chinense fruits. Sci Hortic 112:266–270CrossRefGoogle Scholar
  29. Leister D (2012) How can the light reactions of photosynthesis be improved in plants? Front Plant Sci 3:199PubMedCentralPubMedGoogle Scholar
  30. Ma YT, Wubs AM, Mathieu A, Heuvelink E, Zhu JY, Hu BG, Cournede PH, de Reffye P (2011) Simulation of fruit-set and trophic competition and optimization of yield advantages in six Capsicum cultivars using functional-structural plant modelling. Ann Bot 107:793–803PubMedCentralCrossRefPubMedGoogle Scholar
  31. Marcelis LFM, Heuvelink E, Hofman-Eijer LRB, Den Bakker J, Xue LB (2004) Flower and fruit abortion in sweet pepper in relation to source and sink strength. J Exp Bot 55:2261–2268CrossRefPubMedGoogle Scholar
  32. Meyer RC, Steinfath M, Lisec J, Becher M, Witucka-Wall H, Torjek O, Fiehn O, Eckardt A, Willmitzer L, Selbig J, Altmann T (2007) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:4759–4764PubMedCentralCrossRefPubMedGoogle Scholar
  33. Mitchell-Olds T, Schmitt J (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441:947–952CrossRefPubMedGoogle Scholar
  34. Mojena R (1977) Hierarchical grouping methods and stopping rules—evaluation. Computer J 20:359–363CrossRefGoogle Scholar
  35. Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J 50:1093–1106CrossRefPubMedGoogle Scholar
  36. Nunes-Nesi A, Araujo WL, Fernie AR (2011) Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiol 155:101–107PubMedCentralCrossRefPubMedGoogle Scholar
  37. Onus AN, Pickersgill B (2004) Unilateral incompatibility in Capsicum (Solanaceae): occurrence and taxonomic distribution. Ann Bot 94:289–295PubMedCentralCrossRefPubMedGoogle Scholar
  38. Osorio S, Alba R, Nikoloski Z, Kochevenko A, Fernie AR, Giovannoni JJ (2012) Integrative comparative analyses of transcript and metabolite profiles from pepper and tomato ripening and development stages uncovers species-specific patterns of network regulatory behavior. Plant Physiol 159:1713–1729PubMedCentralCrossRefPubMedGoogle Scholar
  39. Paran I, van der Knaap E (2007) Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. J Exp Bot 58:3841–3852CrossRefPubMedGoogle Scholar
  40. Poorter H, van Rijn CPE, Vanhala TK, Verhoeven KJF, de Jong YEM, Stam P, Lambers H (2005) A genetic analysis of relative growth rate and underlying components in Hordeum spontaneum. Oecologia 142:360–377CrossRefPubMedGoogle Scholar
  41. Pyl ET, Piques M, Ivakov A, Schulze W, Ishihara H, Stitt M, Sulpice R (2012) Metabolism and growth in Arabidopsis depend on the daytime temperature but are temperature-compensated against cool nights. Plant Cell 24:2443–2469PubMedCentralCrossRefPubMedGoogle Scholar
  42. Rao GU, Ben Chaim A, Borovsky Y, Paran I (2003) Mapping of yield-related QTLs in pepper in an interspecific cross of Capsicum annuum and C. frutescens. Theor Appl Genet 106:1457–1466PubMedGoogle Scholar
  43. Reifschneider FJB (2000) Capsicum—Pimentas e Pimentões no Brasil. Embrapa Comunicação para Transferência de Tecnologia/Embrapa Hortaliças. BrasíliaGoogle Scholar
  44. Rodriguez JM, Berke T, Engle L, Nienhuis J (1999) Variation among and within Capsicum species revealed by RAPD markers. Theor Appl Genet 99:147–156CrossRefGoogle Scholar
  45. Schauer N, Semel Y, Balbo I, Steinfath M, Repsilber D, Selbig J, Pleban T, Zamir D, Fernie AR (2008) Mode of inheritance of primary metabolic traits in tomato. Plant Cell 20:509–523PubMedCentralCrossRefPubMedGoogle Scholar
  46. Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell M (eds) Ecophysiology of photosynthesis, vol 100. Springer, Berlin Heidelberg, pp 49–70CrossRefGoogle Scholar
  47. Searle SR (1971) Linear models. John Wiley & Sons, Inc., New YorkGoogle Scholar
  48. Stewart C Jr, Kang BC, Liu K, Mazourek M et al (2005) The Pun1 gene for pungency in pepper encodes a putative acyltransferase. Plant J 42:675–688CrossRefPubMedGoogle Scholar
  49. Stewart C Jr, Mazourek M, Stellari GM, O’Connell M, Jahn M (2007) Genetic control of pungency in C. chinense via the Pun1 locus. J Exp Bot 58:979–991CrossRefPubMedGoogle Scholar
  50. Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M, Witucka-Wall H, Gibon Y, Usadel B, Poree F, Piques MC, Von Korff M, Steinhauser MC, Keurentjes JJ, Guenther M, Hoehne M, Selbig J, Fernie AR, Altmann T, Stitt M (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci USA 106:10348–10353PubMedCentralCrossRefPubMedGoogle Scholar
  51. Sulpice R, Trenkamp S, Steinfath M, Usadel B, Gibon Y, Witucka-Wall H, Pyl ET, Tschoep H, Steinhauser MC, Guenther M, Hoehne M, Rohwer JM, Altmann T, Fernie AR, Stitt M (2010) Network analysis of enzyme activities and metabolite levels and their relationship to biomass in a large panel of Arabidopsis accessions. Plant Cell 22:2872–2893PubMedCentralCrossRefPubMedGoogle Scholar
  52. Sulpice R, Nikoloski Z, Tschoep H, Antonio C, Kleessen S, Larhlimi A, Selbig J, Ishihara H, Gibon Y, Fernie AR, Stitt M (2013) Impact of the carbon and nitrogen supply on relationships and connectivity between metabolism and biomass in a broad panel of arabidopsis accessions. Plant Physiol 162:347–363PubMedCentralCrossRefPubMedGoogle Scholar
  53. Trontin C, Tisne S, Bach L, Loudet O (2011) What does Arabidopsis natural variation teach us (and does not teach us) about adaptation in plants? Curr Opin Plant Biol 14:225–231CrossRefPubMedGoogle Scholar
  54. Turner AD, Wien HC (1994) Dry-matter assimilation and partitioning in pepper cultivars differing in susceptibility to stress-induced bud and flower abscission. Ann Bot 73:617–622CrossRefGoogle Scholar
  55. Valantin-Morison M, Vaissiere BE, Gary C, Robin P (2006) Source–sink balance affects reproductive development and fruit quality in cantaloupe melon (Cucumis melo L.). J Horticult Sci Biotechnol 81:105–117Google Scholar
  56. von Groll U (2002) The subtilisin-like serine protease SDD1 mediates cell-to-cell signaling during Arabidopsis stomatal development. Plant Cell 14:1527–1539CrossRefGoogle Scholar
  57. Wahyuni Y, Ballester AR, Sudarmonowati E, Bino RJ, Bovy AG (2011) Metabolite biodiversity in pepper (Capsicum) fruits of thirty-two diverse accessions: variation in health-related compounds and implications for breeding. Phytochemistry 72:1358–1370CrossRefPubMedGoogle Scholar
  58. Wahyuni Y, Ballester AR, Sudarmonowati E, Bino RJ, Bovy AG (2013a) Secondary metabolites of Capsicum species and their importance in the human diet. J Nat Prod 76:783–793CrossRefPubMedGoogle Scholar
  59. Wahyuni Y, Ballester AR, Tikunov Y, de Vos RCH et al (2013b) Metabolomics and molecular marker analysis to explore pepper (Capsicum sp.) biodiversity. Metabolomics 9:130–144PubMedCentralCrossRefPubMedGoogle Scholar
  60. Wahyuni Y, Stahl-Hermes V, Ballester AR et al (2014) Genetic mapping of semi-polar metabolites in pepper fruits (Capsicum sp.): towards unravelling the molecular regulation of flavonoid quantitative trait loci. Mol Breed 33:503–518PubMedCentralCrossRefPubMedGoogle Scholar
  61. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedCentralPubMedGoogle Scholar
  62. Wubs AM, Ma Y, Heuvelink E, Marcelis LFM (2009) Genetic differences in fruit-set patterns are determined by differences in fruit sink strength and a source : sink threshold for fruit set. Ann Bot 104:957–964PubMedCentralCrossRefPubMedGoogle Scholar
  63. Zhu X-G, de Sturler E, Long SP (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol 145:513–526PubMedCentralCrossRefPubMedGoogle Scholar
  64. Zygier S, Chaim AB, Efrati A, Kaluzky G, Borovsky Y, Paran I (2005) QTLs mapping for fruit size and shape in chromosomes 2 and 4 in pepper and a comparison of the pepper QTL map with that of tomato. Theor Appl Genet 111:437–445CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Laise Rosado-Souza
    • 1
  • Federico Scossa
    • 2
    • 3
  • Izabel S. Chaves
    • 1
  • Sabrina Kleessen
    • 2
  • Luiz F. D. Salvador
    • 1
  • Jocimar C. Milagre
    • 1
  • Fernando Finger
    • 4
  • Leonardo L. Bhering
    • 5
  • Ronan Sulpice
    • 6
  • Wagner L. Araújo
    • 1
  • Zoran Nikoloski
    • 2
  • Alisdair R. Fernie
    • 2
  • Adriano Nunes-Nesi
    • 1
    Email author
  1. 1.Max-Planck Partner Group at the Departamento de Biologia VegetalUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Max-Planck-Institute of Molecular Plant PhysiologyPotsdam-GolmGermany
  3. 3.Consiglio per la Ricerca e la Sperimentazione in AgricolturaResearch Center for Fruit ScienceRomeItaly
  4. 4.Departamento de FitotecniaUniversidade Federal de ViçosaViçosaBrazil
  5. 5.Departamento de Biologia GeralUniversidade Federal de ViçosaViçosaBrazil
  6. 6.Plant Systems Biology Lab, Plant and AgriBiosciences Research Centre, Botany and Plant ScienceNational University of IrelandGalwayIreland

Personalised recommendations