Metabolic acclimation supports higher aluminium-induced secretion of citrate and malate in an aluminium-tolerant hybrid clone of Eucalyptus

Abstract

Background Eucalyptus is the main plantation wood species, mostly grown in aluminized acid soils. To understand the response of Eucalyptus clones to aluminum (Al) toxicity, the Al-tolerant Eucalyptus grandis × E. urophylla clone GL-9 (designated “G9”) and the Al-sensitive E. urophylla clone GL-4 (designated “W4”) were employed to investigate the production and secretion of citrate and malate by roots. Results Eucalyptus seedlings in hydroponics were exposed to the presence or absence of 4.4 mM Al at pH 4.0 for 24 h. The protein synthesis inhibitor cycloheximide (CHM) and anion channel blocker phenylglyoxal (PG) were applied to explore possible pathways involved in organic acid secretion. The secretion of malate and citrate was earlier and greater in G9 than in W4, corresponding to less Al accumulation in G9. The concentration of Al in G9 roots peaked after 1 h and decreased afterwards, corresponding with a rapid induction of malate secretion. A time-lag of about 6 h in citrate efflux in G9 was followed by robust secretion to support continuous Al-detoxification. Malate secretion alone may alleviate Al toxicity because the peaks of Al accumulation and malate secretion were simultaneous in W4, which did not secrete appreciable citrate. Enhanced activities of citrate synthase (CS) and phosphoenolpyruvate carboxylase (PEPC), and reduced activities of isocitrate dehydrogenase (IDH), aconitase (ACO) and malic enzyme (ME) were closely associated with the greater secretion of citrate in G9. PG effectively inhibited citrate and malate secretion in both Eucalyptus clones. CHM also inhibited malate and citrate secretion in G9, and citrate secretion in W4, but notably did not affect malate secretion in W4. Conclusions G9 immediately secrete malate from roots, which had an initial effect on Al-detoxification, followed by time-delayed citrate secretion. Pre-existing anion channel protein first contributed to malate secretion, while synthesis of carrier protein appeared to be needed for citrate excretion. The changes of organic acid concentrations in response to Al can be achieved by enhanced CS and PEPC activities, but was supported by changes in the activities of other enzymes involved in organic acid metabolism. The above information may help to further explore genes related to Al-tolerance in Eucalyptus.

Effects of Elevated Aluminum Concentration and Distribution on Root Damage, Cell Wall Polysaccharides, and Nutrient Uptake in Different Tolerant Eucalyptus Clones

“…However, there was a significant lag in the secretion of organic acids by the root tips of G4. This proves that organic acids contribute to the Al tolerance of Eucalyptus , and the accumulation and secretion of organic acids in cells are involved in Al detoxification [ 43 ].…”

Exogenous silicon induces aluminum tolerance in white clover (Trifolium repens) by reducing aluminum uptake and enhancing organic acid secretion

“…One common mechanism by which plants protect themselves against aluminum (Al) toxicity is the exudation of organic acids. However, the reasons behind the different types of organic acids that various plant species secrete remain unknown ( Li et al, 2009 , 2021 ; Ma, 2000 ; Ryan et al, 2009 ). So far, it has been determined that the primary organic acid anions released by plant roots in response to aluminum stress are citrate, malate, and oxalate ( Sun et al, 2020b ).…”