APPLICATION OF NITROGEN COMBINED WITH TRICHODERMA HARZIANUM IN SUGAR APPLE AND CUSTARD APPLE SEEDLINGS

Authors

DOI:

https://doi.org/10.32404/rean.v13i1.10221

Keywords:

Annona squamosa L., Annona reticulata L., Trichoderma spp., Bioinputs

Abstract

This study aimed to evaluate the growth-promoting potential of Trichoderma harzianum in sugar apple (Annona squamosa L.) and custard apple (Annona reticulata L.) seedlings. The seedlings were subjected to different nitrogen rates combined with Trichoderma application strategies. The design used was a randomized complete block, with a 3 × 5 factorial arrangement of Trichoderma application strategy and nitrogen rates, and three replications. The Trichoderma application strategy included: S1 – control (no application); S2 – IBLF 006 WP applied at planting; and S3 – IBLF 006 WP applied at planting and again 30 days after seedling emergence. Evaluated variables included relative chlorophyll index (RCI), chlorophyll a (Chl a), chlorophyll b (Chl b), plant height (PH), number of leaves (NL), shoot fresh mass (SFM), and shoot dry mass (SDM). In sugar apple, Trichoderma increased shoot dry mass by 29.4% (S2) and 16.8% (S3) in the absence of nitrogen of fertilization and promoted greater plant height at low rates (0–25 kg ha-¹). In custard apple, S3 resulted in higher fresh and dry shoot biomass, particularly at low (0–25 kg ha-¹ N) and high (75–100 kg ha-¹ N) nitrogen rates. The application of strain IBLF 006 (Trichoderma harzianum) is not recommended for the production of sugar apple (Annona squamosa L.) and custard apple (Annona reticulata L.) seedlings, either alone or in combination with different nitrogen rates, as the observed benefits were limited and inconsistent. Therefore, under the experimental conditions, a nitrogen rate of 100 kg ha-¹ provided the best overall results and is recommended for nursery seedling production.

Author Biographies

  • Natália Veleda Duailibe, Universidade Estadual de Goiás, Unidade de Ipameri, Ipameri, Goiás, Brasil.

    Universidade Estadual de Goiás, Unidade de Ipameri, Ipameri, Goiás, Brasil.

  • Rikelme Matheus dos Santos Relvas, Universidade Federal de Viçosa, Departamento de Agronomia, Viçosa, Minas Gerais, Brasil.

    Universidade Federal de Viçosa, Departamento de Agronomia, Viçosa, Minas Gerais, Brasil.

  • Rithielly Machado Rodrigues de Araújo , Universidade Estadual de Goiás, Unidade de Ipameri, Ipameri, Goiás, Brasil.

    Universidade Estadual de Goiás, Unidade de Ipameri, Ipameri, Goiás, Brasil.

  • Luciana Maria da Silva, Instituto Federal Goiano, Campus Rio Verde, Rio Verde, Goiás, Brasil.

    Instituto Federal Goiano, Campus Rio Verde, Rio Verde, Goiás, Brasil.

  • Fabrício Rodrigues, Universidade Estadual de Goiás, Unidade de Ipameri, Ipameri, Goiás, Brasil.

    Universidade Estadual de Goiás, Unidade de Ipameri, Ipameri, Goiás, Brasil.

References

(I) Abdelmoaty, S., Khandaker, M.M., Mahmud, K., Majrashi, A., Alenazi, M.M., Badaluddin, N.A., 2022. Influence of Trichoderma harzianum and Bacillus thuringiensis with reducing rates of NPK on growth, physiology and fruit quality of Citrus aurantifolia. Brazilian Journal of Biology, 82, e261032. https://doi.org/10.1590/1519-6984.261032

(II) Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L. M., and Sparovek, G., 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22, 711–728.

(III) Anozie, E.L., Egwunatum, A.E., Igbinosa, I.O., Umeh, C.L., Udeze, U., 2023. Evaluating the effects of biochar and organic soil amendments on seedling development of Annona muricata Linn. Asian Journal of Research in Agriculture and Forestry, 9(1), 1–9.

(IV) Araújo, J.F., 2007. Adubação organomineral e biofertilização líquida na produção de frutos de pinha (Annona squamosa L.) no submédio São Francisco. Tese (Doutorado) – Universidade Estadual Paulista “Júlio de Mesquita Filho”, Repositório UNESP, Botucatu, Brasil.

(V) Araújo, R.C., Babilônia, G. B., Mendes, L. S., Reis, J.M.R., 2019. Uso de Trichoderma harzianum na produção de mudas de mamoeiro. Cerrado Agrociências, 10, 86-95.

(VI) Batista, M.M.F., Viégas, I.D.J.M., Frazão, D.A.C., Thomaz, M.A.A., Silva, R.D.C.L.D., 2003. Effect of macronutrient omission in growth, symptoms of nutritional deficiency and mineral composition in soursop plants (Annona muricata). Revista Brasileira de Fruticultura, 25(2), 315–318.

(VII) Bjorn, L.O., Papageorgiou, G.C., Blankenship, R.E., Govindjee., 2009. A viewpoint: why chlorophyll a? Photosynthesis Research, 99, 85–98. https://doi.org/10.1007/s11120-008-9395-x

(VIII) Brannan, R., O’Neal, D., Jawad, M., 2025. Characterization of carotenoids and color in temperate Asimina triloba and comparison to other tropical Annonaceae fruits. Exploration of Foods and Foodomics, 3, 101098. https://doi.org/10.37349/eff.2025.101098

(IX) Brasil. Ministério do Meio Ambiente (MMA). 2022. Portaria MMA nº 148, de 7 de junho de 2022. Diário Oficial da União, Brasília, Brasil.

(X) Cavalcante, A.L.A., Negreiros, A.M.P., Melo, N.J.D.A., Santos, F.J.Q., Soares Silva, C.S.A., Pinto, P.S.L., Sales Júnior, R., 2025. Adaptability and sensitivity of Trichoderma spp. isolates to environmental factors and fungicides. Microorganisms, 13(7), 1689. https://doi.org/10.3390/microorganisms13071689

(XI) CBI. Centre for the Promotion of Imports. 2024. The European market potential for exotic fruit. CBI, The Hague, Netherlands.

(XII) Chen, M., 2014. Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Annual Review of Biochemistry, 83, 317–340. https://doi.org/10.1146/annurev-biochem-072711-162943

(XIII) Costa, A.M., Carlos, L., Silva, P. O., Barbosa, K. P., Rodrigues, C. R., 2019. Nitrogen and Potassium Fertilization in the Initial Growth of Annona crassiflora Mart. Floram, 26(2), 1-9. https://doi.org/10.1590/2179-8087.034117

(XIV) Couvreur, T.L., Helmstetter, A.J., Koenen, E.J., Bethune, K., Brandão, R.D., Little, S.A., Erkens, R.H., 2019. Phylogenomics of the major tropical plant family Annonaceae using targeted enrichment of nuclear genes. Frontiers in Plant Science, 9, 1941. https://doi.org/10.3389/fpls.2018.01941

(XV) FAO. 2020. Fruit and vegetables – your dietary essentials: The international year of fruits and vegetables, 2021, Background paper. Food and Agriculture Organization of the United Nations, Rome, Italy.

(XVI) Faria, R.A.N., Pereira, M.C.T., Cordeiro, R.A., Pimenta, S., Nietsche, S., Silva, J.F., 2025. Phenotypic characterization of progenies from the cross of atemoya with red-skinned sugar apple. Fruit Crops Science Journal, 1, e-878, 1-10.

(XVII) Ferreira, D.F., 2011. Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia, 35, 1039–1042. https://doi.org/10.1590/S1413-70542011000600001

(XVIII) Fuentes, L.M., Montalvo González, E., García Magaña, M.L., Anaya Esparza, L.M., Nolasco González, Y., Villagrán, Z., 2022. Current situation and perspectives of fruit Annonaceae in Mexico: biological and agronomic importance and bioactive properties. Plants, 11(1), 7. https://doi.org/10.3390/plants11010007

(XIX) Hermosa, R., Rubio, M.B., Cardoza, R.E., Nicolás, C., Monte, E., Gutiérrez, S., 2013. The contribution of Trichoderma to balancing the costs of plant growth and defense. International Microbiology, 16, 69–80. https://doi.org/10.2436/20.1501.01.181

(XX) Huang, Y., Li, D., Liu, X., Ren, Z., 2024. Monitoring canopy SPAD based on UAV and multispectral imaging over fruit tree growth stages and species. Frontiers in Plant Science, 15, 1435613. https://doi.org/10.3389/fpls.2024.1435613

(XXI) IBGE. 2024. PAM 2024: Com queda nos preços e na safra de grãos, valor da produção agrícola cai pelo segundo ano seguido. Agência IBGE Notícias, Rio de Janeiro, Brasil.

(XXII) Lemos, E.E.P., 2014. Produção de frutos de annona no Brasil. Revista Brasileira de Fruticultura, 36(edição especial), 77–85. https://doi.org/10.1590/S0100-29452014000500009

(XXIII) Liu, K.D., Yuan, C.C., Jing, G.X., Li, H.L., Liu, J.X., 2013. Effect of exogenous oxalic acid treatment on ripening and preservation of Annona squamosa L. fruits during postharvest storage. Food Science, 14, 329–334.

(XXIV) Liu, Z., Xu, N., Pang, Q., Khan, R.A.A., Xu, Q., Wu, C., Liu, T., 2023. A salt-tolerant strain of Trichoderma longibrachiatum HL167 is effective in alleviating salt stress, promoting plant growth, and managing Fusarium wilt disease in cowpea. Journal of Fungi, 9(3), 304. https://doi.org/10.3390/jof9030304

(XXV) Meneses, F.J.R., de Oliveira Lopes, Á.L., Setubal, I.S., da Costa Neto, V.P., Bonifácio, A., 2022. Inoculation of Trichoderma asperelloides ameliorates aluminum stress-induced damages by improving growth, photosynthetic pigments and organic solutes in maize. 3 Biotech, 12, 246. https://doi.org/10.1007/s13205-022-03311-2

(XXVI) Morton, M.J., Awlia, M., Al-Tamimi, N., Saade, S., Pailles, Y., Negrão, S., Tester, M., 2019. Salt stress under the scalpel – dissecting the genetics of salt tolerance. The Plant Journal, 97, 148–163. https://doi.org/10.1111/tpj.14189

(XXVII) Niaz, N., Gulzar, S., Kazmi, J.H., Aleem, S.A., Pham, M.P.P., Mierzwa-Hersztek, M.M.H., Mushtaq, Z.N., 2024. Assessment of chlorophyll content in leaves of crops and orchards based on SPAD, multispectral, and hyperspectral techniques. Ecological Questions, 35(2), 161–174. https://doi.org/10.12775/EQ.2024.018

(XXVIII) Poveda, J., 2020. Trichoderma parareesei favors the tolerance of rapeseed (Brassica napus L.) to salinity and drought due to a chorismate mutase. Agronomy, 10, 118. https://doi.org/10.3390/agronomy10010118

(XXIX) Paraginski, J.A., Moraes, M.P., Carlos, F., Mayer, N.A., Bianchi, V.J., 2025. Trichoderma asperellum and mineral fertilization improve chlorophyll content and growth of Prunus persica L. batsch rootstocks. Plant and Soil, 1-18. https://doi.org/10.1007/s11104-025-07453-z

(XXX) Rodriguez-Gomez, D., Hobley, T.J., 2013. Is an organic nitrogen source needed for cellulase production by Trichoderma reesei Rut-C30? World Journal of Microbiology and Biotechnology, 29, 2157–2165. https://doi.org/10.1007/s11274-013-1381-6

(XXXI) Sá, F.V.S., Gheyi, H.R., de Lima, G.S., Pinheiro, F.W.A., de Paiva, E.P., Moreira, R.C.L., Fernandes, P.D., 2021. The right combination of NPK fertilization may mitigate salt stress in custard apple (Annona squamosa L.). Acta Physiologiae Plantarum, 43, 59. https://doi.org/10.1007/s11738-021-03225-1

(XXXII) Santos, H.G., Jacomine, P.K.T., Anjos, L.H.C., Oliveira, V.A., Lumbreras, J.F., Coelho, M.R., Almeida, J.A., Araujo Filho, J.C., Oliveira, J.B., Cunha, T.J.F., 2018. Sistema Brasileiro de Classificação de Solos. 5ª ed. Embrapa, Brasília, Brasil.

(XXXIII) Santos, J.M.R., Silva, R.A., Taniguchi, C.A.K., Silva, C.F.B., Natale, W., Artur, A.G., 2021. Trichoderma spp. in the promotion of growth and nutrition of dwarf cashew rootstocks. Revista Ciência Agronômica, 52(4), e20207697. https:// doi.org/10.5935/1806-6690.20210053

(XXXIV) Singh, S.P., Pandey, S., Mishra, N., Giri, V.P., Mahfooz, S., Bhattacharya, A., Mishra, A., 2019. Supplementation of Trichoderma improves the alteration of nutrient allocation and transporter genes expression in rice under nutrient deficiencies. Plant Physiology and Biochemistry, 143, 351–363. https://doi.org/10.1016/j.plaphy.2019.09.015

(XXXV) Sousa, W.N., Brito, N.F., Felsemburgh, C.A., Vieira, T.A.; Lustosa, D.C., 2021. Evaluation of Trichoderma spp. isolates in cocoa seed treatment and seedling production. Plants, 10 (9), 1964, 1-10. https://doi.org/10.3390/plants10091964

(XXXVI) Teixeira, N., Melo, J.C., Batista, L.F., Paula-Souza, J., Fronza, P., Brandão, M.G., 2019. Edible fruits from Brazilian biodiversity: a review on their sensorial characteristics versus bioactivity as tool to select research. Food Research International, 119, 325–348. https://doi.org/10.1016/j.foodres.2019.01.058

(XXXVII) Vindas-Reyes, E., Chacón-Cerdas, R., Rivera-Méndez, W., 2024. Trichoderma production and encapsulation methods for agricultural applications. AgriEngineering, 6(3), 2366–2384. https://doi.org/10.3390/agriengineering6030138

(XXXVIII) Wei, L., Lu, L., Shang, Y., Ran, X., Liu, Y., Fang, Y., 2024. Can SPAD values and CIE L a b scales predict chlorophyll and carotenoid concentrations in leaves and diagnose the growth potential of trees? Horticulturae, 10(6), 548. https://doi.org/10.3390/horticulturae10060548

(XXXIX) Zhu, H., Dardick, C.D., Beers, E.P., Callahan, A.M., Xia, R., Yuan, R., 2011. Transcriptomics of shading-induced and NAA-induced abscission in apple (Malus domestica) reveals a shared pathway involving reduced photosynthesis, alterations in carbohydrate transport and signaling and hormone crosstalk. BMC Plant Biology, 11, 138. https://doi.org/10.1186/1471-2229-11-138

(XL) Zydlik, Z., Zydlik, P., Wieczorek, R., 2021. The effects of bioinoculants based on mycorrhizal and Trichoderma spp. fungi in an apple tree nursery under replantation conditions. Agronomy, 11(11), 2355. https://doi.org/10.3390/agronomy11112355

Downloads

Published

2026-09-25

How to Cite

APPLICATION OF NITROGEN COMBINED WITH TRICHODERMA HARZIANUM IN SUGAR APPLE AND CUSTARD APPLE SEEDLINGS. (2026). REVISTA DE AGRICULTURA NEOTROPICAL, 13(1). https://doi.org/10.32404/rean.v13i1.10221