Adaptive Responses of Citrus grandis Leaves to Copper Toxicity Revealed by RNA-Seq and Physiology

Abstract

Copper (Cu)-toxic effects on Citrus grandis growth and Cu uptake, as well as gene expression and physiological parameters in leaves were investigated. Using RNA-Seq, 715 upregulated and 573 downregulated genes were identified in leaves of C. grandis seedlings exposed to Cu-toxicity (LCGSEC). Cu-toxicity altered the expression of 52 genes related to cell wall metabolism, thus impairing cell wall metabolism and lowering leaf growth. Cu-toxicity downregulated the expression of photosynthetic electron transport-related genes, thus reducing CO2 assimilation. Some genes involved in thermal energy dissipation, photorespiration, reactive oxygen species scavenging and cell redox homeostasis and some antioxidants (reduced glutathione, phytochelatins, metallothioneins, l-tryptophan and total phenolics) were upregulated in LCGSEC, but they could not protect LCGSEC from oxidative damage. Several adaptive responses might occur in LCGSEC. LCGSEC displayed both enhanced capacities to maintain homeostasis of Cu via reducing Cu uptake by leaves and preventing release of vacuolar Cu into the cytoplasm, and to improve internal detoxification of Cu by accumulating Cu chelators (lignin, reduced glutathione, phytochelatins, metallothioneins, l-tryptophan and total phenolics). The capacities to maintain both energy homeostasis and Ca homeostasis might be upregulated in LCGSEC. Cu-toxicity increased abscisates (auxins) level, thus stimulating stomatal closure and lowering water loss (enhancing water use efficiency and photosynthesis).

Molecular and Physiological Responses of Citrus sinensis Leaves to Long-Term Low pH Revealed by RNA-Seq Integrated with Targeted Metabolomics

“…Interestingly, the levels of Trp, Orn, Phe, and Pro in leaves were increased by low pH ( Figure 4 A). This agreed with the reports that low pH increased the concentration of Pro in wheat leaves at grain filling [ 12 ] and pea leaves [ 53 ], that drought increased the levels of Phe, Trp, and Pro in leaves of maize hybrids [ 54 ], and that Cu-toxicity improved the levels of Phe, Trp, indole-3-acetic acid (IAA), and total auxins in C. grandis leaves [ 17 , 55 ]. In plants, Pro is biosynthesized by two pathways, the Orn and Glu pathways.…”

“…RNA-Seq has been widely applied to investigate abiotic stress-induced alterations of gene expression in plants, including aluminum (Al) and heavy metal toxicities, as well as nutrient stresses [ 14 , 15 , 16 , 17 , 18 ]. Although the physiological responses of leaves to low pH have been investigated in some detail, less information was available about low pH-responsive genes.…”

Comparative Transcriptome Analysis Reveals Complex Physiological Response and Gene Regulation in Peanut Roots and Leaves under Manganese Toxicity Stress

“…In recent years, high-throughput transcriptome sequencing technology has been extensively employed to study the response mechanisms of plants to toxic stresses of heavy metals, such as copper, lead, aluminum, and cadmium, including Citrus grandis , Raphanus sativus , O. sativa , and Saccharum officinarum [ 29 , 30 , 31 , 32 ]. However, limited studies have focused on manganese-induced stress in peanut plants, and the molecular regulatory mechanism of peanut plants in response to Mn stress remains unknown.…”

Physiological and Ultrastructural Responses to Excessive-Copper-Induced Toxicity in Two Differentially Copper Tolerant Citrus Species

“…Revealing the Cu-tolerant mechanisms of citrus species is crucial for optimized Cu-nutrient management and for improving environmental quality in the sustainable development of citrus production. For those purposes, we have investigated the Cu tolerance of citrus seedlings at the biochemical and physiological [ 16 ], transcriptional [ 17 ], proteomic [ 18 ] and metabolomic levels [ 19 ]. Our previous findings indicate that activated antioxidative defenses [ 19 ] promote Cu retention by the root cell wall [ 20 ] and secretion of root exudates [ 21 ] represented the most critical responses to Cu toxicity in citrus species.…”