Rootstock, scion, and microbiome contributions to cadmium mitigation in five Indonesian cocoa cultivars.

Main Article Content

Jennifer Elise Schmidt
https://orcid.org/0000-0001-7403-5829
Mikael Dorman
Andrew Ward
Alana Firl

Abstract

Reducing levels of heavy metals such as cadmium (Cd) in cacao beans has become an important priority for cacao production in Indonesia. Current mitigation strategies revolve around breeding and the use of soil ameliorants, and in the future, the soil microbiome may also have the potential to reduce Cd bioavailability and uptake by cacao trees. However, there remains a need for locally specific recommendations for low-Cd-accumulating cacao cultivars and knowledge of native beneficial bacteria and fungi. In a greenhouse study using field soil supplemented with Cd, five cacao clones (MCC02, M01, S1, S2, and ICCRI 9) were grafted in a fully factorial design to the same hybrid half sibling rootstocks, plant uptake was measured before and after the addition of cadmium nitrate, and rhizosphere microbial communities were characterized. Rootstock, scion, and graft combinations all significantly affected plant Cd levels, but the ranking of clones differed between low and high Cd soils. Twenty-six bacterial taxa and one fungal taxon were associated with Cd uptake. These results highlight the continued importance of breeding as a cadmium mitigation strategy and support the potential for the soil microbiome to contribute to reducing cadmium uptake in cacao.

Article Details


How to Cite
Schmidt, J., Dorman, M., Ward, A., & Firl, A. (2023). Rootstock, scion, and microbiome contributions to cadmium mitigation in five Indonesian cocoa cultivars. Pelita Perkebunan (a Coffee and Cocoa Research Journal), 39(3), 201-215. https://doi.org/10.22302/iccri.jur.pelitaperkebunan.v39i3.555
Section
Articles
Creative Commons License

This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.

Authors who publish with this journal agree to the following terms:

    1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
    1. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
    1. Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).

 

References
Abarenkov, K., Zirk, A., Piirmann, T., Pöhönen, R., Ivanov, F., Nilsson, R. H., et al. (2020). UNITE general FASTA release for Fungi. Version 04.02.2020. UNITE Community. Available at: https://doi.org/10.15156/BIO/786368 [Accessed April 7, 2021].
American Public Health Association (1992). “APHA Method 3120,” in Standard Methods for the Examination of Water and Wastewater, ed. M. A. H. Franson (Washington, D.C.), 3.34-3.40.
AOAC Official Method 2015.01 Heavy Metals in Food (n.d.). Available at: www.perkinelmer.com [Accessed May 17, 2023].
Basotra, N., Kaur, B., Di Falco, M., Tsang, A., and Chadha, B. S. (2016). Mycothermus thermophilus (Syn. Scytalidium thermophilum): Repertoire of a diverse array of efficient cellulases and hemicellulases in the secretome revealed. Bioresour Technol 222, 413–421. doi: 10.1016/J.BIORTECH.2016.10.018.
Bernard, A. (2008). Cadmium & its adverse effects on human health. Indian J Med Res 128, 557–564. Available at: https://journals.lww.com/ijmr/_layouts/15/oaks.journals/downloadpdf.aspx?an=02223309-200828040-00016 [Accessed May 9, 2023].
Bravo, D., Pardo-Díaz, S., Benavides-Erazo, J., Rengifo-Estrada, G., Braissant, O., and Leon-Moreno, C. (2018). Cadmium and cadmium-tolerant soil bacteria in cacao crops from northeastern Colombia. J Appl Microbiol 124, 1175–1194. doi: 10.1111/jam.13698.
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., and Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13, 581–583. doi: 10.1038/nmeth.3869.
Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Lozupone, C. A., Turnbaugh, P. J., et al. (2011). Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108, 4516–4522. doi: 10.1073/pnas.1000080107.
Chen, B., Zhang, Y., Rafiq, M. T., Khan, K. Y., Pan, F., Yang, X., et al. (2014). Improvement of cadmium uptake and accumulation in Sedum alfredii by endophytic bacteria Sphingomonas SaMR12: Effects on plant growth and root exudates. Chemosphere 117, 367–373. doi: 10.1016/J.CHEMOSPHERE.2014.07.078.
Cheng, C., Wang, R., Sun, L., He, L., and Sheng, X. (2021). Cadmium-resistant and arginine decarboxylase-producing endophytic Sphingomonas sp. C40 decreases cadmium accumulation in host rice (Oryza sativa Cliangyou 513). Chemosphere 275, 130109. doi: 10.1016/J.CHEMOSPHERE.2021.130109.
Cordoba-Novoa, H. A., Cáceres-Zambrano, J., and Torres-Rojas, E. (2022). Assessment of native cadmium-tolerant bacteria in cacao (Theobroma cacao L.)-cultivated soils in Cundinamarca-Colombia. doi: 10.21203/rs.3.rs-1726295/v1.
EC No 488/2014 (2014).
Fahmid, I. M., Harun, H., Fahmid, M. M., Saadah, and Busthanul, N. (2018). Competitiveness, production, and productivity of cocoa in Indonesia. IOP Conf Ser Earth Environ Sci 157, 012067. doi: 10.1088/1755-1315/157/1/012067.
Fahmid, I. M., Wahyudi, Salman, D., Kariyasa, I. K., Fahmid, M. M., Agustian, A., et al. (2022). “Downstreaming” Policy Supporting the Competitiveness of Indonesian Cocoa in the Global Market. Front Sustain Food Syst 6, 204. doi: 10.3389/FSUFS.2022.821330/BIBTEX.
Gardes, M., and Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes ‐ application to the identification of mycorrhizae and rusts. Mol Ecol 2, 113–118. doi: 10.1111/j.1365-294X.1993.tb00005.x.
Guerra Sierra, B., Arteaga-Figueroa, L., Sierra-Pelaéz, S., and Alvarez, J. (2022). Talaromyces santanderensis: a New Cadmium-tolerant Fungus from Cacao Soils in Colombia. doi: 10.20944/PREPRINTS202208.0185.V1.
International Cocoa Organization (2023). Production of Cocoa Beans (thousand tonnes). ICCO Quarterly Bulletin of Cocoa Statistics XLIX.
Kubier, A., Wilkin, R. T., and Pichler, T. (2019). Cadmium in soils and groundwater: A review. Appl Geochem 108, 1. doi: 10.1016/J.APGEOCHEM.2019.104388.
Kumar, P., Edelstein, M., Cardarelli, M., Ferri, E., and Colla, G. (2015). Grafting Affects Growth, Yield, Nutrient Uptake, and Partitioning Under Cadmium Stress in Tomato. HortScience 50, 1654–1661. doi: 10.21273/HORTSCI.50.11.1654.
Liu, Y., Xiao, T., Perkins, R. B., Zhu, J., Zhu, Z., Xiong, Y., et al. (2017). Geogenic cadmium pollution and potential health risks, with emphasis on black shale. J Geochem Explor 176, 42–49. doi: 10.1016/J.GEXPLO.2016.04.004.
Mallick, H., Rahnavard, A., McIver, L. J., Ma, S., Zhang, Y., Nguyen, L. H., et al. (2021). Multivariable association discovery in population-scale meta-omics studies. PLoS Comput Biol 17, e1009442. doi: 10.1371/JOURNAL.PCBI.1009442.
Meter, A., Atkinson, R. J., and Laliberte, R. (2019). Cadmium in Cacao from Latin America and the Caribbean: A Review of Research and Potential Mitigation Solutions. Rome Available at: https://scioteca.caf.com/bitstream/handle/123456789/1506/Cadmium_in_Cacao_From_Latin_America_and_The_Caribbean.pdf?sequence=1&isAllowed=y [Accessed May 7, 2023].
Muehe, E. M., Weigold, P., Adaktylou, I. J., Planer-Friedrich, B., Kraemer, U., Kappler, A., et al. (2015). Rhizosphere Microbial Community Composition Affects Cadmium and Zinc Uptake by the Metal-Hyperaccumulating Plant Arabidopsis halleri. Appl Environ Microbiol 81, 2173–2181. doi: 10.1128/AEM.03359.
Nilsson, R. H., Larsson, K. H., Taylor, A. F. S., Bengtsson-Palme, J., Jeppesen, T. S., Schigel, D., et al. (2019). The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47, D259–D264. doi: 10.1093/NAR/GKY1022.
Oksanen, J., Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, et al. (2022). vegan: Community Ecology Package.
Pan, F., Meng, Q., Wang, Q., Luo, S., Chen, B., Khan, K. Y., et al. (2016). Endophytic bacterium Sphingomonas SaMR12 promotes cadmium accumulation by increasing glutathione biosynthesis in Sedum alfredii Hance. Chemosphere 154, 358–366. doi: 10.1016/J.CHEMOSPHERE.2016.03.120.
Pinheiro, J., and Bates, D. (2022). nlme: Linear and Nonlinear Mixed Effects Models.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res 41, D590–D596. doi: 10.1093/nar/gks1219.
Quiroga-Mateus, R., López-Zuleta, S., Chávez, E., and Bravo, D. (2022). Cadmium-Tolerant Bacteria in Cacao Farms from Antioquia, Colombia: Isolation, Characterization and Potential Use to Mitigate Cadmium Contamination. Processes 10, 1457. doi: 10.3390/pr10081457.
R Core Team (2022). R: A Language and Environment for Statistical Computing. Available at: https://www.r-project.org/.
Ramtahal, G., Yen, I. C., Bekele, I., Bekele, F., Wilson, L., Maharaj, K., et al. (2016). Relationships between Cadmium in Tissues of Cacao Trees and Soils in Plantations of Trinidad and Tobago. Food Nutr Sci 7, 37–43. doi: 10.4236/FNS.2016.71005.
Schmidt, J. E., DuVal, A., Puig, A., Tempeleu, A., and Crow, T. (2021). Interactive and Dynamic Effects of Rootstock and Rhizobiome on Scion Nutrition in Cacao Seedlings. Frontiers in Agronomy 0, 89. doi: 10.3389/FAGRO.2021.754646.
SNI 7386-2009 (2009). Badan Standardisasi Nasional.
Tangaromsuk, J., Pokethitiyook, P., Kruatrachue, M., and Upatham, E. S. (2002). Cadmium biosorption by Sphingomonas paucimobilis biomass. Bioresour Technol 85, 103–105. doi: 10.1016/S0960-8524(02)00066-4.
U.S. EPA (1996). EPA Method 3050B: Acid Digestion of Sediments, Sludges, and Soils. Revision 2. Available at: https://www.epa.gov/esam/epa-method-3050b-acid-digestion-sediments-sludges-and-soils [Accessed May 17, 2023].
White, T. J., Bruns, T., Lee, S., and Taylor, J. W. (1990). “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,” in PCR Protocols: A Guide to Methods and Applications, eds. M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White (New York: Academic Press, Inc.), 315–322.
Wu, B., Li, J., Peng, D., Wang, Z., and Xu, H. (2022). Cadmium Exposure Alters Rhizospheric Microbial Community and Transcriptional Expression of Vetiver Grass. Front Plant Sci 13. doi: 10.3389/fpls.2022.808844.
Wyszkowska, J., Boros-Lajszner, E., Borowik, A., and Kucharski, J. (2022). The Role of Cellulose in Microbial Diversity Changes in the Soil Contaminated with Cadmium. Sustainability 14, 14242. doi: 10.3390/SU142114242.
Xie, Y., Tan, H., Sun, G., Li, H., Liang, D., Xia, H., et al. (2020). Grafting Alleviates Cadmium Toxicity and Reduces Its Absorption by Tomato. J Soil Sci Plant Nutr 20, 2222–2229. doi: 10.1007/S42729-020-00289-9/TABLES/6.
Yilmaz, P., Parfrey, L. W., Yarza, P., Gerken, J., Pruesse, E., Quast, C., et al. (2014). The SILVA and “all-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res 42, D643–D648. doi: 10.1093/nar/gkt1209.
Zakariyya, F., Santoso, T. I., and Abdoellah, S. (2022). Absorption of Cadmium and its Effect on the Growth of Halfsib Family of Three Cocoa Clones Seedling. Pelita Perkebunan (a Coffee and Cocoa Research Journal) 38, 171–178. doi: 10.22302/ICCRI.JUR.PELITAPERKEBUNAN.V38I3.534.