Dynamics of photosynthetic responses in 10 rubber tree (Hevea brasiliensis) clones in Colombian Amazon: Implications for breeding strategies

Autoři: Armando Sterling aff001;  Natalia Rodríguez aff001;  Esther Quiceno aff001;  Faiver Trujillo aff001;  Andrés Clavijo aff001;  Juan Carlos Suárez-Salazar aff002
Působiště autorů: Laboratorio de Fitopatología, Instituto Amazónico de Investigaciones Científicas Sinchi–Facultad de Ciencias Básicas—Universidad de la Amazonía, Florencia, Colombia aff001;  Laboratorio de Ecofisiología, Universidad de la Amazonia, Facultad de Ingeniería, Programa de Ingeniería Agroecológica, Florencia-Caquetá, Colombia aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226254


The rubber tree [Hevea brasiliensis (Willd. Ex Adr. de Juss.) Muell.-Arg] is the main source of natural rubber in the world. However, in the Amazon region, its production is reduced by biotic and abiotic limitations, which have prompted breeding programs in order to identify desirable agronomic and physiological indicators. The objective of this study was to analyze the temporal dynamics of photosynthetic responses based on the parameters of leaf gas exchange and chlorophyll a fluorescence in 10 rubber tree clones during the immature phase (pre-tapping) in three large-scale clone trials, during daily cycles and under two climatic periods (dry and rainy) in the Caquetá region (Colombian Amazon). The variables A, LT, ΦPSII, ETR and qP were significantly higher in the dry period, where the highest values of PAR, AT and VPD were seen. In San Vicente del Caguán and Florencia, the highest averages were estimated for A, E and gs, as compared with Belén de los Andaquíes. In Florencia, the highest fluorescence parameters of chlorophyll a were recorded. At 9:00 h and 12:00 h, the highest means of A, E, ΦPSII and ETR were observed. The majority of the clones displayed the highest Fv/Fm mean (0.82–0.84) in the dry period. The clones FX 4098, FDR 4575, MDF 180, GU198 and FDR 5788 represent genotypes with the best photosynthetic performance (greater photosynthetic rates and better ability of the photosynthetic apparatus to capture, use and dissipate light energy). These desirable genotypes constitute a promising gene pool for expanding the genetic resource of rubber trees in the Colombian Amazon.

Klíčová slova:

Chlorophyll – Leaves – Light – Photosynthesis – Rubber – Stomata – Photochemistry


1. Venkatachalam P, Geetha N, Sangeetha P, Thulaseedharan A. Natural rubber producing plants: An overview. African J Biotechnol. 2013;12: 1297–1310. doi: 10.5897/AJBX12.016

2. International Rubber Study Group (IRSG). Rubber Statiscal Bulletin. Sri Lanka; 2019.

3. Goncalves P de S, Ortolani AA, Cardoso M. Melhoramento genetico da seringueira: uma revisao [Internet]. Instituto Agronomico, Campinas (Brazil): Instituto Agronomico, Campinas (Brazil); 1997. Available: http://agris.fao.org/agris-search/search.do?recordID=XF2015009815

4. Falqueto AR, da Silva Júnior RA, Gomes MTG, Martins JPR, Silva DM, Partelli FL. Effects of drought stress on chlorophyll a fluorescence in two rubber tree clones. Sci Hortic (Amsterdam). 2017;224: 238–243. doi: 10.1016/j.scienta.2017.06.019

5. Ping L, Jun-jun H, Yan-li Y, Xiao-hong D, Ru-xiong C, Li-feng W. Differential responses of two rubber tree clones to chilling stress. African J Biotechnol. 2012;11: 13466–13471. doi: 10.5897/AJB12.1180

6. Miguel AA, Oliveira LEM de, Cairo PAR, Oliveira DM de. Photosynthetic behaviour during the leaf ontogeny of rubber tree clones[Hevea brasiliensis (Wild. ex. Adr. de Juss.) Muell. Arg.]. Ciênc Agrotec Lavras. 2007;31: 91–97. doi: 10.1590/S1413-70542007000100014

7. Sterling A, Melgarejo LM. Leaf gas exchange and chlorophyll a fluorescence in Hevea brasiliensis in response to Pseudocercospora ulei infection. Physiol Mol Plant Pathol. Elsevier Ltd; 2018;103: 143–150. doi: 10.1016/j.pmpp.2018.07.006

8. Nataraja KN, Jacob J. Clonal differences in photosynthesis in Hevea brasiliensis Müll. Arg. Photosynthetica. 1999;36: 89–98. https://doi.org/10.1023/A:1007070820925

9. Nugawela A, Long SP, Aluthhewage RK. Genotypic variation in non-steady state photosynthetic carbon dioxide assimilation of Hevea brasiliensis. J Rubber Res Inst Sri Lanka. 1995;10: 266–275.

10. Ahmad B, Idris H, Sulong SH. Early Selection of Promising High Yielding Hevea Progenies based on Selected Physiological and. J Rubber Res. 2009;12: 140–150.

11. Sterling A, Rodríguez CH. Ampliación de la base genética de caucho natural con proyección para la Amazonia colombiana: fase de evaluación en periodo improductivo a gran escala. Bogotá: Instituto Amazónico de Investigaciones Científicas- Sinchi; 2012.

12. Bacelar EA, Santos DL, Moutinho-Pereira JM, Gonçalves BC, Ferreira HF, Correia CM. Immediate responses and adaptative strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci. 2006;170: 596–605.

13. Rodrigo VHL. Ecophysiological factors underpinning productivity of Hevea brasiliensis. Brazilian J Plant Physiol. 2007;19: 245–255. doi: 10.1590/S1677-04202007000400002

14. Senevirathna AMWK, Stirling CM, Rodrigo VHL. Growth, photosynthetic performance and shade adaptation of rubber (Hevea brasiliensis) grown in natural shade. Tree Physiol. 2003;23: 705–712. doi: 10.1093/treephys/23.10.705 12777243

15. Ávila C, Murillo R, Hernández C, Flores G, Murillo O, Arias D. Photosynthetic Behavior of Gmelina Arborea Genotypes in Rooted Mini-Cuttings Stage under Nursery Conditions, at South Pacific of Costa Rica. Int J Appl Sci Technol. 2017;7: 32–44.

16. DaMatta F, Chaves A, Pinheiro H, Ducatti C, Loureiro M. Drought tolerance of two field-grown clones of Coffea canephora Drought tolerance of two field-grown clones of Coffea canephora. Plant Sci. 2003;164: 111–117. doi: 10.1016/S0168-9452(02)00342-4

17. Granda V, Delatorre C, Cuesta C, Centeno ML, Fernández B, Rodríguez A, et al. Physiological and biochemical responses to severe drought stress of nine Eucalyptus globulus clones: A multivariate approach. Tree Physiol. 2014;34: 778–786. doi: 10.1093/treephys/tpu052 25009154

18. Espinoza SE, Magni CR, Rubilar RA, Yañez MA, Santelices RE, Cabrera AM, et al. Field performance of various Pinus radiata breeding families established on a drought-prone site in central Chile. New Zeal J For Sci. 2017;47: 12. doi: 10.1186/s40490-017-0093-3

19. Zhao X, Li Y, Zheng M, Bian X, Liu M, Sun Y, et al. Comparative analysis of growth and photosynthetic characteristics of (Populus simonii × P. nigra) × (P. nigra × P. simonii) hybrid clones of different ploidides. PLoS One. 2015;10: 1–16. doi: 10.1371/journal.pone.0119259 25867100

20. Holá D, Benešová M, Honnerová J, Hnilička F, Rothová O, Kočová M, et al. The evaluation of photosynthetic parameters in maize inbred lines subjected to water deficiency: Can these parameters be used for the prediction of performance of hybrid progeny? Photosynthetica. 2010;48: 545–558. doi: 10.1007/s11099-010-0072-x

21. Brestic M, Zivcak M, Hauptvogel P, Misheva S, Kocheva K, Yang X, et al. Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. Photosynth Res. Springer Netherlands; 2018;136: 245–255. doi: 10.1007/s11120-018-0486-z 29383631

22. Huang D, Wu L, Chen JR, Dong L. Morphological plasticity, photosynthesis and chlorophyll fluorescence of Athyrium pachyphlebium at different shade levels. Photosynthetica. 2011;49: 611–618. doi: 10.1007/s11099-011-0076-1

23. Murchie EH, Lawson T. Chlorophyll fluorescence analysis: A guide to good practice and understanding some new applications. J Exp Bot. 2013;64: 3983–3998. doi: 10.1093/jxb/ert208 23913954

24. Dai Y, Shen Z, Liu Y, Wang L, Hannaway D, Lu H. Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ Exp Bot. 2009;65: 177–182. doi: 10.1016/j.envexpbot.2008.12.008

25. Tcherkez G, Limami AM. Net photosynthetic CO2 assimilation: more than just CO2 and O2 reduction cycles. New Phytol. 2019;223: 520–529. doi: 10.1111/nph.15828 30927445

26. Priyadarshan PM. Biology of Hevea Rubber. 1st ed. Priyadarshan PM, editor. Springer International Publishing; 2017. doi: 10.1007/978-3-319-54506-6

27. Instituto Geográfico Agustin Codazzi (IGAC). Caquetá, características geográficas. Bogotá, DC: Imprenta nacional de Colombia; 2010.

28. Murad CA, Pearse J. Landsat study of deforestation in the Amazon region of Colombia: Departments of Caquetá and Putumayo. Remote Sens Appl Soc Environ. Elsevier; 2018;11: 161–171. doi: 10.1016/J.RSASE.2018.07.003

29. Instituto de Hidrología Meteorología y Estudios Ambientales (IDEAM). Promedios precipitación y temperatura media. Promedio de los años 1981–2015. In: Instituto de Hidrología Meteorología y Estudios Ambientales. 2015.

30. Corpoamazonia. Clima del Caquetá—Región sur [Internet]. 2013. Available: http://www.corpoamazonia.gov.co/region/Jur_Clima.htm

31. Le Guen V, Garcia D, Mattos CRR, Clément-Demange A. Evaluation of field resistance to Microcyclus ulei of a collection of Amazonian rubber tree (Hevea brasiliensis) germplasm. Crop Breed Appl Biotechnol. 2002;2: 141–148.

32. Garcia D, Mattos CRR, Gonçalves P de S, Le Guen V. Selection of Rubber Clones for Resistance to South American Leaf Blight and Latex Yield in the Germplasm of the Michelin Plantation of Bahia (Brazil). J Rubber Res. 2004;7: 188–198.

33. Cardoso SEA, Freitas TA, Da C. Silva D, Gouvêa LRL, Gonçalves PDS, Mattos CRR, et al. Comparison of growth, yield and related traits of resistant Hevea genotypes under high South American leaf blight pressure. Ind Crops Prod. 2014;53: 337–349. doi: 10.1016/j.indcrop.2013.12.033

34. Rivano F, Martinez M, Cevallos V, Cilas C. Assessing resistance of rubber tree clones to Microcyclus ulei in large-scale clone trials in Ecuador: A less time-consuming field method. Eur J Plant Pathol. 2010;126: 541–552. doi: 10.1007/s10658-009-9563-7

35. Confederación Cauchera Colombiana (CCC). Estado actual del gremio cauchero colombiano. Bogotá, Colombia; 2015.

36. Clément-Demange A, Nicolas D, Legnaté H, Rivano F, Le Guen V, Gnagne M, et al. Hévéa: stratégies de sélection. Plant Rech Développement. 1995;2: 5–14.

37. Marino G, Aqil M, Shipley B. The leaf economics spectrum and the prediction of photosynthetic light–response curves. Funct Ecol. 2010;24: 263–272. doi: 10.1111/j.1365-2435.2009.01630.x

38. Cuevas E, Baeza P, Lissarrague JR. Variation in stomatal behaviour and gas exchange between mid-morning and mid-afternoon of north-south oriented grapevines (Vitis vinifera L. cv. Tempranillo) at different levels of soil water availability. Sci Hortic (Amsterdam). 2006;108: 173–180. doi: 10.1016/j.scienta.2006.01.027

39. Hallé F, Oldeman RAA, Tomlinson PB. Tropical trees and forest. Berlin, DE; 1978.

40. Baker NR. Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo. Annu Rev Plant Biol. 2008;59: 89–113. doi: 10.1146/annurev.arplant.59.032607.092759 18444897

41. Maxwell K, Johnson GN. Chlorophyll fluorescence—a practical guide. J Exp Bot. 2000;51: 659–668. doi: 10.1093/jxb/51.345.659 10938857

42. Genty B, Briantais J, Baker NR. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta. 1989;990: 87–92.

43. Di Rienzo JA, Macchiavelli RE, Casanoves F. Modelos lineales mixtos: aplicaciones en InfoStat. Córdoba, Argentina; 2011.

44. Pinheiro J, Bates D, Saikat D. Deepayan Sarkar and the R development core team. Nlme: Linear and Nonlinear Mixed Effects Models. R packageversion. 2013. pp. 1–109.

45. R. Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria: R Foundation for statistical Computing; 2017. Available: http://www.r-project.org/

46. Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW. InfoStat versión (2017) [Internet]. Córdoba, Ar.: Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina; 2017. Available: http://www.infostat.com.ar

47. Dolédec S, Chessel D. Co‐inertia analysis: an alternative method for studying species–environment relationships. Freshw Biol. 1994;31: 277–294. doi: 10.1111/j.1365-2427.1994.tb01741.x

48. Thioulouse J, Chessel D, Dolédec S, Olivier J-M. ADE-4 a Multivariate Analysis and Graphical Display Software. Stat Comput. 1997;7. doi: 10.1023/A:1018513530268

49. Renninger HJ, Phillips N. Wet-vs. Dry-Season Transpiration in an Amazonian Rain Forest Palm Iriartea deltoidea. Biotropica. 2010;42: 470–478. doi: 10.1111/j.1744-7429.2009.00612.x

50. Zhang JL, Meng LZ, Cao KF. Sustained diurnal photosynthetic depression in uppermost-canopy leaves of four dipterocarp species in the rainy and dry seasons: Does photorespiration play a role in photoprotection? Tree Physiol. 2009;29: 217–228. doi: 10.1093/treephys/tpn018 19203947

51. Lawson T, Vialet-Chabrand S. Speedy stomata, photosynthesis and plant water use efficiency. New Phytol. 2019;221: 93–98. doi: 10.1111/nph.15330 29987878

52. Vongcharoen K, Santanoo S, Banterng P, Jogloy S, Vorasoot N, Theerakulpisut P. Seasonal variation in photosynthesis performance of cassava at two different growth stages under irrigated and rain-fed conditions in a tropical savanna climate. Photosynthetica. 2018;56: 1398–1413. doi: 10.1007/s11099-018-0849-x

53. Kositsup B, Kasemsap P, Thanisawanyangkura S, Chairungsee N, Satakhun D, Teerawatanasuk K, et al. Effect of leaf age and position on light-saturated CO2 assimilation rate, photosynthetic capacity, and stomatal conductance in rubber trees. Photosynthetica. 2010;48: 67–78. doi: 10.1007/s11099-010-0010-y

54. Ribeiro R V., Machado EC, Santos MG, Oliveira RF. Seasonal and diurnal changes in photosynthetic limitation of young sweet orange trees. Environ Exp Bot. 2009;66: 203–211. doi: 10.1016/j.envexpbot.2009.03.011

55. Guan K, Pan M, Li H, Wolf A, Wu J, Medvigy D, et al. Photosynthetic seasonality of global tropical forests constrained by hydroclimate. Nat Geosci. 2015;8: 284–289. doi: 10.1038/ngeo2382

56. Wu J, Albert LP, Lopes AP, Restrepo-Coupe N, Hayek M, Wiedemann KT, et al. Leaf development and demography explain photosynthetic seasonality in Amazon evergreen forests. Science (80-). 2016;351: 972–976. doi: 10.1126/science.aad5068 26917771

57. Morton DC, Nagol J, Carabajal CC, Rosette J, Palace M, Cook BD, et al. Amazon forests maintain consistent canopy structure and greenness during the dry season. Nature. Nature Publishing Group; 2014;506: 221–224. doi: 10.1038/nature13006 24499816

58. Wujeska-Klause A, Bossinger G, Tausz M. Responses to heatwaves of gas exchange, chlorophyll fluorescence and antioxidants ascorbic acid and glutathione in congeneric pairs of Acacia and Eucalyptus species from relatively cooler and warmer climates. Trees—Struct Funct. Springer Berlin Heidelberg; 2015;29: 1929–1941. doi: 10.1007/s00468-015-1274-4

59. Restrepo-Coupe N, da Rocha HR, Hutyra LR, da Araujo AC, Borma LS, Christoffersen B, et al. What drives the seasonality of photosynthesis across the Amazon basin? A cross-site analysis of eddy flux tower measurements from the Brasil flux network. Agric For Meteorol. Elsevier B.V.; 2013;182–183: 128–144. doi: 10.1016/j.agrformet.2013.04.031

60. Verbeeck H, Peylin P, Bacour C, Bonal D, Steppe K, Ciais P. Seasonal patterns of CO 2 fluxes in Amazon forests: Fusion of eddy covariance data and the ORCHIDEE model. J Geophys Res. 2011;116: 1–19. doi: 10.1029/2010jg001544

61. Gunasekera HKLK, Costa W a JMDE, Nugawela A. Canopy Photosynthetic Capacity and Light Response Parameters of Rubber Hevea brasiliensis with. Curr Agric Res J. 2013;1: 1–12.

62. Ding L, Wang KJ, Jiang GM, Li YG, Jiang CD, Liu MZ, et al. Diurnal variation of gas exchange, chlorophyll fluorescence, and xanthophyll cycle components of maize hybrids released in different years. Photosynthetica. 2006;44: 26–31. doi: 10.1007/s11099-005-0154-3

63. Yao X, Li C, Li S, Zhu Q, Zhang H, Wang H, et al. Effect of shade on leaf photosynthetic capacity, light-intercepting, electron transfer and energy distribution of soybeans. Plant Growth Regul. Springer Netherlands; 2017;83: 409–416. doi: 10.1007/s10725-017-0307-y

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