Cynara cardunculus L. as a Multipurpose Crop for Plant Secondary Metabolites Production in Marginal Stressed Lands

Abstract

Cardoon (Cynara cardunculus L.) is a Mediterranean crop, member of the Asteraceae family, characterized by high production of biomass and secondary metabolites and by a good adaptation to climate change, usable in green chemistry, nutraceutical, and pharmaceutical sectors. Recent studies demonstrated the ability of cardoon to grow up in a stressful environment, which is associated with enhanced biosynthesis of biologically active compounds in these plants, and this effect is increased by abiotic stresses (salt, heat, pollution, and drought stress) that characterize many world marginal areas, affected by the climate changes. The plant response to these stresses consists in implementing different processes that modify some plant biological functions, such as alleviating both cellular hyperosmolarity and ion disequilibrium or synthesizing antioxidant molecules. The aim of this work was to investigate different cardoon response mechanisms to abiotic stresses and to evaluate their influence on the biologically active compounds biosynthesis. Following this purpose, we analyzed the ability of cardoon seeds to germinate under different salt stress conditions, and on the sprouts obtained, we measured the total phenol content and the antioxidant activity. Moreover, the growth of cardoon seedlings grown under heavy metals stress conditions was monitored, and the expression levels of heavy metal transport-associated genes were analyzed. The results showed the ability of cardoon plants to tolerate abiotic stress, thanks to different defense mechanisms and the possibility to obtain biomass with high content of biologically active molecules by exploiting the natural tolerance of this species for abiotic stresses. Moreover, we identified some important genes encoding for metal transportation that may be involved in arsenic and cadmium uptake and translocation in C. cardunculus. Then, this species can be considered as a promising crop for green chemistry and energy in marginal lands.

Keywords: antioxidant activity; gene expression; heavy metals; salt; sprout.

FIGURE 1

Fresh weight (A) and dry weight (B) percentage of altilis sprouts grown at different salt concentrations (0, 60, and 120 mM). The error bars represent the error mean of three biological replicates. Different letters indicate differences at P ≤ 0.05 (ANOVA).

FIGURE 2

Total phenol content (A) and antioxidant activity (B) of altilis sprouts grown in at different salt concentrations (0, 60, and 120 mM). The error bars represent the error mean of three biological replicates. Different letters indicate differences at P ≤ 0.05 (ANOVA).

FIGURE 3

Root and shoot lengths of sylvestris (A) and altilis (B) harvested after 21 days of treatment under different concentrations of As and Cd. The error bars indicate the standard deviation of three biological replicates.

FIGURE 4

The level of gene expression of NRAMP3 in seedlings of altilis and sylvestris grown up to 2 and 3 weeks under Cd (A,B) and As (C,D) at different concentrations. The fold change is the Ct value with respect to the housekeeping genes (EF1α and GAPDH) that is considered 1. The error bars represent the error mean of three biological replicates. Letters indicate only significantly different values (P ≤ 0.05) between concentrations in each moment of sampling.

FIGURE 5

The level of gene expression of ZIP11 in seedlings of altilis and sylvestris grown up to 2 and 3 weeks under Cd (A,B) and As (C,D) at different concentrations. The fold change is the Ct value with respect to the housekeeping genes (EF1α and GAPDH) that is considered 1. The error bars represent the error mean of three biological replicates. Letters indicate only significantly different values (P ≤ 0.05) between concentrations in each moment of sampling.

FIGURE 6

The level of gene expression of HMA in seedlings of altilis and sylvestris grown up to 2 and 3 weeks under Cd (A,B) and As (C,D) at different concentrations. The fold change is the Ct value with respect to the housekeeping genes (EF1α and GAPDH) that is considered 1. The error bars represent the error mean of three biological replicates. Letters indicate only significantly different values (P ≤ 0.05) between concentrations in each moment of sampling.

FIGURE 7

The level of gene expression of PHT in seedlings of altilis and sylvestris grown up to 2 and 3 weeks under Cd (A,B) and As (C,D) at different concentrations. The fold change is the Ct value with respect to the housekeeping genes (EF1α and GAPDH) that is considered 1. The error bars represent the error mean of three biological replicates. Letters indicate only significantly different values (P ≤ 0.05) between concentrations in each moment of sampling.

FIGURE 8

The level of gene expression of ABCC in seedlings of altilis and sylvestris grown up to 2 and 3 weeks under Cd (A,B) and As (C,D) at different concentrations. The fold change is the Ct value with respect to the housekeeping genes (EF1α and GAPDH) that is considered 1. The error bars represent the error mean of three biological replicates. Letters indicate only significantly different values (P ≤ 0.05) between concentrations in each moment of sampling.

FIGURE 9

Principal component analysis using the RT-qPCR fold-change values of the five metal-response–associated genes along with the shoot and root length.