Cadmium-induced transgenerational effects on tomato plants: A gift from parents to progenies

Marina Lima Nogueira; Marcia Eugenia Amaral Carvalho; João Marcos Martins Ferreira; Leticia Aparecida Bressanin; Katherine Derlene Batagin Piotto; Fernando Angelo Piotto; Deyvid Novaes Marques; Sandro Barbosa; Ricardo Antunes Azevedo

doi:10.1016/j.scitotenv.2021.147885

Cadmium-induced transgenerational effects on tomato plants: A gift from parents to progenies

Sci Total Environ. 2021 Oct 1:789:147885. doi: 10.1016/j.scitotenv.2021.147885. Epub 2021 May 21.

Authors

Marina Lima Nogueira¹, Marcia Eugenia Amaral Carvalho¹, João Marcos Martins Ferreira², Leticia Aparecida Bressanin², Katherine Derlene Batagin Piotto¹, Fernando Angelo Piotto³, Deyvid Novaes Marques¹, Sandro Barbosa², Ricardo Antunes Azevedo⁴

Affiliations

¹ Departamento de Genética, Escola Superior de Agricultura "Luiz de Queiroz"/Universidade de São Paulo (ESALQ/USP), Avenida Pádua Dias, 11, 13418-900, Piracicaba, SP, Brazil.
² Instituto de Ciências da Natureza, Universidade Federal de Alfenas (UNIFAL), Rua Gabriel Monteiro da Silva, 700, Centro, 37130-000, Alfenas, MG, Brazil.
³ Departamento de Produção Vegetal, Escola Superior de Agricultura "Luiz de Queiroz"/Universidade de São Paulo (ESALQ/USP), Avenida Pádua Dias, 11, 13418-900, Piracicaba, SP, Brazil.
⁴ Departamento de Genética, Escola Superior de Agricultura "Luiz de Queiroz"/Universidade de São Paulo (ESALQ/USP), Avenida Pádua Dias, 11, 13418-900, Piracicaba, SP, Brazil. Electronic address: raa@usp.br.

PMID: 34323842
DOI: 10.1016/j.scitotenv.2021.147885

Abstract

The present study aimed to investigate the Cd-induced transgenerational effects on plants. Grafted tomato plants, which exhibited the same cultivar as scion and distinct cultivars with contrasting Cd-tolerance as rootstocks, were grown in soil without and with artificial addition of Cd (less than 2.0, and 6.9 mg kg^-1 of Cd, respectively) in a pot experiment carried out in a greenhouse. Their fruits were harvested to extract seeds (i.e., the progenies), which were sown over either Cd-free (control) or Cd-containing germitest paper (germination testing paper with 0 and 35 μM of CdCl₂, respectively) and grown in a growth chamber. The immediate progeny of all grafting combinations from stressed plants presented an elevated germinability, despite high internal Cd concentration. When sown in Cd-containing germitest paper, the immediate progeny of plants grown in soil with no Cd addition was generally able to maintain or even increase the content of carotenoids and chlorophylls a and b (up to 93.3, 62.8 and 76.1%, respectively), indicating a Cd-induced hormetic effect on photosynthetic pigments. Two of the grafting combinations from stressed plants yielded seeds that generated seedlings with enhanced dry mass when they were sown in Cd-free media (~41%), suggesting a Cd-induced transgenerational enhancement of biomass production. Because only one tomato cultivar was used as scion, data indicated that type and degree of Cd-induced transgenerational effects depend strongly on signals generated and/or processed in roots of the parental plants. When sown in Cd-contaminated germitest paper, the immediate progeny of Cd-treated plants presented major reductions in the leaf area (35-69%) and content of photosynthetic pigments (57-93%) in comparison to the progeny from control plants. However, one of the grafting combinations exhibited satisfactory performance after "double" exposure to Cd, showing 91% of the biomass that was produced in the seedlings of control seeds from control plants. Further investigation indicated that adjustments in the chlorophyll fluorescence behavior might counterbalance losses in leaf pigments and area. Taken together, our data provide new insights on the origin, outcomes and mode of action of the Cd-induced transgenerational effects.

Keywords: Cd; Heavy metal; Hormesis; Photosynthetic apparatus; Seed germination; Solanum lycopersicum.