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

Planta volume 242, pages 677–691 (2015)Cite this article

Abstract

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.

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Abbreviations

Φ PSII :

Actual quantum yield of PSII electron transport

R d :

Dark respiration

DW:

Dry weight

WUE:

Intrinsic water use efficiency

F v/F m :

Maximum photochemical efficiency of PSII

A :

Net carbon assimilation

NPQ :

Non-photochemical quenching

qP :

Photochemical quenching

RGR:

Relative growth rate

SLA:

Specific leaf area

g s :

Stomatal conductance

E :

Transpiration rates

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Acknowledgments

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.

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Authors and Affiliations

  1. Max-Planck Partner Group at the Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil

    Laise Rosado-Souza, Izabel S. Chaves, Luiz F. D. Salvador, Jocimar C. Milagre, Wagner L. Araújo & Adriano Nunes-Nesi

  2. Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam-Golm, Germany

    Federico Scossa, Sabrina Kleessen, Zoran Nikoloski & Alisdair R. Fernie

  3. Consiglio per la Ricerca e la Sperimentazione in Agricoltura, Research Center for Fruit Science, Via di Fioranello 52, 00134, Rome, Italy

    Federico Scossa

  4. Departamento de Fitotecnia, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil

    Fernando Finger

  5. Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil

    Leonardo L. Bhering

  6. Plant Systems Biology Lab, Plant and AgriBiosciences Research Centre, Botany and Plant Science, National University of Ireland, Galway, Ireland

    Ronan Sulpice

Authors
  1. Laise Rosado-Souza
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  2. Federico Scossa
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  3. Izabel S. Chaves
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  4. Sabrina Kleessen
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  5. Luiz F. D. Salvador
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  6. Jocimar C. Milagre
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  7. Fernando Finger
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  9. Ronan Sulpice
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  10. Wagner L. Araújo
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  11. Zoran Nikoloski
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  12. Alisdair R. Fernie
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  13. Adriano Nunes-Nesi
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Corresponding author

Correspondence to Adriano Nunes-Nesi.

Electronic supplementary material

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425_2015_2332_MOESM1_ESM.pdf

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

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)

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Rosado-Souza, L., Scossa, F., Chaves, I.S. et al. Exploring natural variation of photosynthetic, primary metabolism and growth parameters in a large panel of Capsicum chinense accessions. Planta 242, 677–691 (2015). https://doi.org/10.1007/s00425-015-2332-2

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Keywords

  • Capsicum
  • Natural genetic variation
  • Pepper
  • Photosynthesis
  • Primary metabolism
  • Respiration