Mature A. marina propagules used in this experiment were collected from the Longhai Mangrove Natural Reserve, Jiulong River Estuary, Fujian province, China (24°24’ N, 117°55’ E). Propagules were disinfected with 1% (w/v) KMnO₄ and washed with deionized water. High vitality propagules were chosen for further pre-cultivation in sea sands. Propagules with a comparable diameter (2.5 ± 0.5 cm) were selected and transplanted into black polyethylene seedling pots with a modified Hoagland nutrient solution, the formula was adapted from previous study on A. marina (Li et al., 2015). All seedling pots were placed in a greenhouse with a daily temperature of 25 ± 5 °C (60-80% relative humidity, and 12 h dark/light). The nutrient solution was renewed every 3 days until seedlings had 3-4 fully developed leaves. After that, different treatments were introduced.

The experiment process included two stages (as a cycle), iron plaque induction and Cd stress. Each treatment had three replicates. In the first stage, iron plaque on the root surface was induced by using four different levels of FeSO₄·7H₂O: no exogenous Fe (0.02 mmol L^-1 Fe from the nutrient solution as Fe₀), low-dose Fe (0.6 mmol L^-1 Fe, as Fe₁), medium-does Fe (1.2 mmol L^-1 Fe, as Fe₂), and high-does Fe (1.8 mmol L^-1 Fe, as Fe₃). Subsequently, during the Cd stress stage, three levels of Cd (as CdCl₂) were introduced (0 mg L^-1, 0.5 mg L^-1, and 2 mg L^-1 as Cd₀, Cd₁, and Cd₂). The applied doses of Cd and Fe were determined based on previous studies on mangrove species (Dai et al., 2017; Jian et al., 2019). The single cycle lasted eight days, including two days in the first stage and six days in the second. During the experiment, those cycles were repeated five times in the total 40 days culture period.

After 40 days of cultivation in the greenhouse, all A. marina were harvested and washed gently with deionized water. After washing, plants were separated into three parts: roots, stems, and leaves, biomass was measured and partial samples were dried at 80 °C to constant weights for metal element analysis. The remaining leaves and roots samples were used for the biochemical analysis.

Statistical analyses were performed using SPSS Statistics 24 (IBM SPSS Statistics for Windows, IBM Corporation, Armonk, NY, USA). Cd and Fe concentrations were considered fixed effects, with replicates considered random effects. All graphs were plotted using OriginPro 2021b (OriginLab, MA, USA). Differences between data from the various treatments were determined using Duncan’s and LSD multiple comparison tests. Treatments were considered significant when F-test P values were< 0.05. The means reported are the least-squares means ± standard deviation of three replicates.

The biomass of A. marina treated by different Fe supply and Cd stress are shown in Table 2 . Fe treatments alone (without Cd stress) significantly increased all of aboveground biomass (P< 0.05), belowground biomass (P< 0.01), and total biomass (P< 0.01). Cd₁ treatment alone (without Fe supply) did not significantly affect the biomass of A. marina. Conversely, for Cd₂ treatment alone the aboveground biomass (P< 0.01), belowground biomass (P< 0.05), and total biomass (P< 0.01) all significantly decreased. Significant negative correlations were observed between different Cd treatments and aboveground biomass (r = -0.682, P< 0.01), and total biomass (r = -0.598, P< 0.01) regardless of different Fe supplies. Furthermore, Fe and Cd treatment interactions were significant on belowground and total biomass (P< 0.01, P< 0.01, respectively, Table 2 ). Within the same Cd treatment (Cd₀, Cd₁, or Cd₂), the Fe supply generally increased plant biomass (belowground biomass and total biomass) relative to the Fe₀ treatments, and Fe₂ or Fe₃ supply resulted in either similar or greater plant biomass compared with the Fe₁ treated plants. For example, under Cd₂ treatment, the addition of Fe₁, Fe₂, and Fe₃ supply increased belowground biomass by 34.95%, 73.66%, and 51.61%, and total biomass increased by 23.26%, 30.56%, and 29.34%, respectively.

Compared with Cd₀ treated plants, Cd₁ treatment alone had no significant influence on chlorophyll concentration in leaves, and Cd₂ treatment caused a considerable decrease in chlorophyll concentration ( Figure 1 ). Fe₁ (P< 0.05) and Fe₂ (P< 0.05) treatment alone significantly increased chlorophyll concentration in plant leaves, whereas under Fe₃ treatment, the concentration was similar to Fe₀ treated plants. Moreover, under the same Cd stress (Cd₁ or Cd₂), the addition of Fe₁ and Fe₂ treatments increased the chlorophyll concentration, while there was no difference between Fe₀ and Fe₃ treated plants. For example, chlorophyll concentration was lowest in Cd₂ combined with Fe₀ treatment, and with the introduction of Fe₁ and Fe₂ treatments, the chlorophyll concentration in leaves of A. marina increased by 16.27% and 29.93%, respectively. However, Fe₃ treatment decreased chlorophyll concentration to a level similar to that of the Cd₂Fe₀.

Cd was mainly distributed in roots, and only part of Cd migrated to stems and leaves irrespective of different treatments ( Figures 2A, B ), except for the Cd₂Fe₀ treatment, in which Cd concentration was higher in stems than in roots and leaves. Significant two-way interactions from Fe and Cd treatments in TF _{R to S} and TF _{S to L} were observed (P< 0.01, P< 0.01 respectively, Figures 2A, B ). Under Cd₁ (P< 0.01) and Cd₂ (P< 0.01) stress, the addition of Fe remarkably decreased roots to stems translocation factor of Cd, and no significant difference was observed among Fe₁, Fe₂, and Fe₃ treatments under the same Cd stress. Similarly, under Cd₂ stress, the addition of Fe significantly (P< 0.01) decreased the stems to leaves translocation factor of Cd, and the TF _{S to L} further decreased with the increase of Fe supply ( Figure 2B ). However, under Cd₁ treatment combined with Fe₁ and Fe₂ supply, TF _{S to L} did not significantly change, and with Fe₃ supply, TF _{S to L} considerably (P< 0.01) decreased.

Cd treatments alone did not significantly affect Fe concentrations in roots and leaves of A. marina. In contrast, the addition of Fe significantly increased Fe concentrations in all of the roots, stems, and leaves regardless of different Cd treatments (P< 0.01, P< 0.01, and P< 0.01, respectively, Figures 2C–E ), and significant positive correlations were observed between different Fe treatments and Fe concentrations in roots and leaves ( Figure 3 ).

Cd treatment alone significantly affected FCR activity in leaves (P< 0.05) and roots (P< 0.05) of A. marina ( Figure 4 ). In leaves, compared with Cd₀Fe₀, Cd₁Fe₀ treatment resulted in a significant (P< 0.05) higher FCR activity, while under a higher Cd₂ stress, the FCR activity decreased to a similar level to Cd₀Fe₀ treated plants. Fe₁ and Fe₂ treatments alone did not significantly affect the FCR activity in leaves, whereas Fe₃ supply caused a significant (P< 0.05) higher FCR activity. Moreover, there was a significant (P< 0.01) effect of Fe and Cd interaction on FCR activity in leaves. In Fe treated (Fe₁, Fe₂, and Fe₃) plants, Cd₁ stress generally led to higher FCR activity. However, FCR activity in leaves generally decreased under Cd₂ stress compared with Cd₁ treated plants. In roots, Cd₁ stress alone did not significantly affect FCR activity, whereas Cd₂ stress alone resulted in a significant decrease in FCR activity ( Figure 4 ). Fe supply alone significantly (P< 0.01) increased FCR activity, and there was a positive correlation between Fe treatments and roots FCR activity (r = 0.881, P< 0.01). Additionally, the application of Cd stress caused either similar or lower FCR activity in the root of Fe treated plants. For example, roots FCR activity decreased by 19.46% and 19.55% in Cd₁Fe₃ and Cd₂Fe₃ treatments, respectively, compared with Cd₀Fe₃ treatment.

In both leaves (P< 0.05) and roots (P< 0.05) of A. marina, POD activity significantly increased under Cd₁ stress ( Figure 5 ). And compared with Cd₁ treated plants, Cd₂ resulted in a higher POD activity in plant tissues. Fe supply alone led to either similar or greater POD activity, and significant positive correlations were obtained between Fe treatments and POD activity in both leaves (r = 0.872, P< 0.01) and roots (r = 0.942, P< 0.01). Moreover, Fe supplied to Cd treated plants further increased POD activity in leaves. For example, compared with Cd₂Fe₀ treatment, POD activity in leaves increased by 21.25%, 477.47%, and 449.13% in Cd₂Fe₁, Cd₂Fe₂, and Cd₂Fe₃ treatments, respectively, and the POD activity in Cd₂Fe₂ treated plants was the highest (165.73 ± 20.70 U g^-1 FW, Figure 5 ). In roots, Fe supply also increased POD activity, and the highest POD activity was observed in Cd₂ combined with Fe₃ treatment (833.80 ± 29.30 U g^-1 FW, Figure 5 ).

Similar to POD activity, Cd stress caused a considerable increase in leaves (P< 0.01) and roots (P< 0.01) PPO activity. In contrast, Fe supply alone only caused higher PPO activity in roots of A. marina, while PPO activity of leaves was not significantly affected. When under Cd stress, the introduction of Fe supply generally increased the activity of PPO in leaves, while PPO activity in leaves was not significantly affected, except for some increases in Cd₁Fe₃ treated plants. The highest PPO activities in leaves and roots were obtained in Cd₂Fe₂ (827.72 ± 29.12 U g^-1 FW) and Cd₁Fe₃ (733.88 ± 18.29 U g^-1 FW) treatments, respectively.

Cd₁ treatment alone did not result in a considerable difference in total phenolics in leaves and roots, while Cd₂ treatment significantly increased total phenolics in different tissues ( Figure 6 ). In contrast, Fe₁ supply alone significantly (P< 0.05) increased total phenolics in leaves, while no further increase in total phenolics concentration was evident at higher Fe₂ or Fe₃ supply. As for roots, only Fe₂ and Fe₃ treatments generally increased total phenolics. When under Cd₁ (P< 0.05) and Cd₂ (P< 0.01) stress, the application of Fe₁ treatment significantly increased total phenolics in leaves of A. marina, and higher total phenolics concentrations were observed under Fe₂ supply. However, compared with Cd₁Fe₂ and Cd₂Fe₂, total phenolics in Cd₁Fe₃ and Cd₂Fe₃ treated plants significantly (P< 0.05) decreased. The total phenolics concentration in leaves was highest in Cd₂ combined with Fe₂ treatment (77.81 ± 1.51 mg g^-1 DW, Figure 6 ), which accounts for 128.99% of Cd₂Fe₀, 116.00% of Cd₂Fe₁, or 108.31% of Cd₂Fe₃. Additionally, under Cd₁ stress, Fe₁ supply did not significantly affect roots total phenolics, while a higher Fe₂ (P< 0.05) or Fe₃ (P< 0.05) supply significantly increased the concentration. When the level of Cd stress further increased, total phenolics concentrations in roots were not significantly affected by different Fe treatments.

Cd₁ stress alone did not affect total tannin in both leaves and roots, whereas Cd₂ stress resulted in significantly higher total tannin concentrations ( Figure 6 ). Interestingly, with the application of Fe₁ or Fe₂ supply alone, total tannin in tissues exhibited a general increasing trend ( Figure 6 ), but with a higher Fe₃ supply, total tannin in leaves and roots decreased remarkably (P< 0.05, n = 3). Similarly, in leaves treated with Cd, the application of Fe₁ or Fe₂ supply led to a general upward trend in total tannin concentration ( Figure 6 ), whereas Fe₃ supply caused either similar or lower total tannin concentration compared with Fe₂ treated plants. For example, the total tannin concentration in Cd₂Fe₀ treated leaves was 20.49 ± 0.97 mg g^-1 DW, with the application of Fe₁ and Fe₂ supply, the concentration increased to 32.54 ± 2.86 mg g^-1 DW, and 36.07 ± 4.01 mg g^-1 DW, respectively, while in Cd₁Fe₃ the concentration was only 27.74 ± 0.85 mg g^-1 DW. In roots, Fe₁ supply combined with different Cd stress did not affect the total tannin concentration. In contrast, a higher Fe₂ or Fe₃ supply generally increased total tannin concentration in roots under Cd stress ( Figure 6 ).

As shown in Figure 3 , a significant negative correlation was found between Cd treatment levels and chlorophyll concentration in leaves, while positive correlations were found between Cd treatments and POD activity in leaves, PPO activity in all tissues, and phenolic compounds (both total phenolics and tannins) in different tissues. Moreover, positive correlations were also observed between Fe treatment levels and FCR activity, POD activity, and phenolic compounds in both roots and leaves, whereas a negative correlation was observed between Fe treatment levels and TF _{R to S}.

Numerous studies have shown that heavy metals such as Cd could result in considerable growth retardation and biomass reduction in different wetland plants (Guangqiu et al., 2007; Dai et al., 2018; Jian et al., 2019). In the present study, Cd₂ treatment alone resulted in significant biomass reduction ( Table 2 ), while the addition of Cd₁ treatment alone did not significantly affect the biomass of A. marina due to the heavy metal tolerance and self-detoxification mechanisms, and Cd₁ treatment did not reach the threshold of causing biotoxicity (Wu et al., 2022a). In contrast, Fe is a critical nutrient element for plant growth and biomass accumulation and is involved in chlorophyll synthesis, chloroplast development, and other metabolism processes (Yoshihara et al., 2006). Therefore, plant growth and biomass accumulation of A. marina were significantly promoted by Fe supply ( Table 2 ). Moreover, in the current study, increasing the Fe supply under Cd stress significantly alleviated biomass reduction caused by Cd toxicity, and it is particularly evident under Fe₁ and Fe₂ treatments ( Table 2 ). This could be attributed to the following aspects: first, the addition of Fe directly facilitated photosynthesis and other biosynthetic processes related to nutrient assimilation and biomass accumulation (Liu et al., 2017; Sági-Kazár et al., 2021). Second, Fe mediated a series of heavy metal immobilization and detoxification processes in copes such as Oryza sativa (Liu et al., 2017) and Vigna radiata (Biyani et al., 2019) under Cd stress, reduced the accumulation of Pb in roots of Spartina alterniflora, a typical salt marsh plant (Zhang et al., 2020), and ultimately reduced heavy metal stress in plant tissues. In contrast, excess Fe may be unfavorable to plants under heavy metal stress (Jian et al., 2019). To demonstrate these aspects, the Fe-mediated chlorophyll concentration, Cd translocation, and detoxification mechanisms were further studied and discussed.

Photosynthesis is the basis of biomass accumulation and plant growth ( Figure 1 ). However, when under Cd stress, it becomes one of the main targets of Cd toxicity (Dai et al., 2017). Cd stress could damage the ultrastructure of membranes, reduce the activity of protochlorophyllide reductase, inhibit the biosynthesis of chlorophyll, and eventually cause the disturbance of photosynthesis (Stobart et al., 1985; Benavides et al., 2005). In this study, Cd₁ treatment had no significant effect on the chlorophyll concentration due to most of Cd accumulated in roots, while the accumulation of Cd in leaves did not reach the level of causing severe damage. However, a higher Cd₂ treatment resulted in a significantly decreased chlorophyll concentration. Furthermore, in plant tissues, Cd competes with Fe for ion channels and enzyme active sites and leads to the disruption of intracellular metabolism (Chang et al., 2003; Liu et al., 2020). The introduction of Fe supply not only directly increased the Fe bioavailability in leaves ( Figure 2E ) and enhanced its competitiveness with Cd, but also restricted the translocation of Cd ( Figures 2A, B ), therefore restoring the synthesis of chlorophyll under Cd stress, and inducing an increase in chlorophyll concentration. On the contrary, excess Fe may not be favorable to plant metabolism and growth (Müller et al., 2017; Mehrabanjoubani et al., 2019). Thus, Fe₁ and Fe₂ treatments significantly increased chlorophyll concentration under different Cd treatments, whereas compared with Fe₂ treated plants, Fe₃ treatment resulted in a decreased chlorophyll concentration ( Figure 1 ).

The present study showed that under Cd₁ stress, both TF _{R to S} and TF_{S to L} were lower than 1 ( Figures 2A, B ), which indicated most Cd was accumulated in roots. In comparison, under Cd₂ stress, most Cd was accumulated in stems. Nevertheless, Cd concentration in leaves was the lowest among all tissues, regardless of different treatments. This could be partly attributed to the redistribution strategy of plant tissues, which allows plants to fix most heavy metals in roots and stems to protect the sensitive leaves (Weng et al., 2012; Wu et al., 2022b). Li et al. (Li et al., 2019a) found that in Aegiceras corniculatum roots, Cd tended to accumulate in xylem and pith, which have a high affinity for Cd and restrict the further translocation of Cd from roots to other tissues. Moreover, under Cd₁ and Cd₂ stress, Fe supply remarkably decreased the translocation of Cd from roots to other tissues ( Figures 2A, B ), and negative correlations between Fe supply and TF _{R to S}, and TF _{S to L} were observed in A. marina (r = -0.695, P< 0.01, and r = -0.513, P< 0.05 respectively), which is comparable to previous research that showed the application of exogenous Fe strongly suppressed the translocation of Cd in different plant species (Sharma et al., 2004; Jian et al., 2019; Liu et al., 2020). These results could be interpreted from three aspects: 1) higher Fe supply significantly enhanced the formation of iron plaque on the root surface of wetland plants, especially mangroves (Liu et al., 2017; Lin et al., 2018). The iron plaque might be a “barrier” inhibiting the uptake and accumulation of heavy metals by roots and hence decrease the amount of heavy metals being translocated to other tissues (Du et al., 2013; Mei et al., 2021). 2) Fe supply convincingly promoted the uptake of Fe by plants and enhanced the accumulation of Fe in different tissues ( Figures 2C–E ), which can cause competitive effects on Cd uptake and translocation (Jian et al., 2019; Wu et al., 2022b). 3) the exogenous Fe supply could not only alleviate the photosynthesis inhibition caused by Cd toxicity ( Figure 1 ) but also help maintain the stable intracellular environment via inducing the upregulating of antioxidant enzymes activities and stimulating the biosynthesis of antioxidant and chelating compounds, which include tannins and other phenolic compounds (Yan and Tam, 2011; Wang et al., 2014; Chen et al., 2019). The chelate effect mediated by tannins and other phenolic compounds play a critical role in restricting the translocation of Cd in plant tissues (Lavid et al., 2001a; Guangqiu et al., 2007; Jiang et al., 2017). Therefore, to further demonstrate the restriction and detoxification effects mediated by Fe, the Fe-induced activities of FCR and typical antioxidant enzymes, as well as the concentrations of total tannin and phenolics were determined and further discussed.

For plants that obtain Fe via the strategy I (also known as the reducing strategy) mechanism, the FCR, which reduces ferric (Fe³⁺) to ferrous (Fe²⁺), plays a critical role in Fe uptake and assimilation by roots (Jeong and Connolly, 2009; Li et al., 2019b). Then, Fe is transported from roots to aboveground tissues via xylem as Fe³⁺-citrate and other complexes (Brüggemann et al., 1993). Subsequently, Fe³⁺ can be reduced by membrane-bound FCR and utilized by leaf cells, which may have high iron requirements due to the biosynthesis of Fe-containing enzymes associated with photosynthesis (Hell and Stephan, 2003). In the present study, the addition of Fe supply promoted the activity of FCR in both roots and leaves. This may be because, in the current study, the first stage is iron plaque induction, in which the Fe supply enhanced the formation of iron plaque and stimulated the activity of FCR ( Figure 4 ). This iron oxide/hydroxide structure can not only adsorb or co-precipitate heavy metals but also be an irrefutable Fe source for plant growth (Sebastian and Prasad, 2016). Moreover, significant positive correlations between FCR activity and Fe concentration were observed in both roots and leaves of A. marina ( Figure 3 ), this further demonstrated the key role of FCR in the uptake of Fe. Additionally, Cd stress had different effects on FCR activity, depending mainly on stress level and plant species. For example, in the study by Bari et al. (Bari et al., 2019), under hydroponic conditions, the addition of 10 uM CdSO₄ significantly increased the FCR activity in roots of O. sativa due to the Cd-caused Fe deficiency. In contrast, for Cucumis sativus, 10 uM or higher level of Cd(NO₃)₂ significantly decreased the FCR activity due to Cd inhibited the biosynthesis of FCR or occupied active binding sites of enzymes (Chang et al., 2003; Kovács et al., 2010). In the present study, Cd concentration in leaves under Cd₁ stress was relatively low due to most Cd was immobilized in roots, these low-level Cd may stimulate the FCR activity, while Cd₂ treatment caused a higher Cd accumulation and biotoxicity in leaves, and hence the FCR activity was inhibited compared to Cd₁ treated leaves. In comparison, for roots, both Cd₁ and Cd₂ treatments negatively impacted FCR activity ( Figure 4 ), this can be attributed to roots directly exposed to Cd solution, and the high toxicity excessed the tolerance threshold of roots and resulted in a decrease in FCR activity.

POD and PPO are typical antioxidant enzymes that respond rapidly under heavy metal stress (Yan and Tam, 2011). The introduction of Cd stress can cause the overproduction and accumulation of ROS, including hydrogen peroxide, superoxide, hydroxyl radicals, and peroxyl radicals (Jiang et al., 2017), and may trigger the antioxidation and detoxification mechanisms in plants. Thus, in this study, Cd led to a higher POD and PPO activity in different tissues compared with Cd₀ treated plants ( Figure 5 ). Additionally, Fe is a well-known cofactor of different antioxidant enzymes (Liu et al., 2020). Therefore, although under Cd stress, the moderate (Fe₁ and Fe₂) Fe supply could maintain the stability of antioxidative systems and scavenge the overgenerated ROS ( Figure 5 ). However, a high or excess Fe can motivate the generation and accumulation of ROS and stimulate a dramatic increase in POD activity (Liu et al., 2017). Similar results were obtained in the present study that Fe₃ supply resulted in a several-fold increase in POD activity in both leaves and roots of A. marina ( Figure 5 ). Besides, the addition of Cd resulted in a significantly higher PPO activity ( Figure 5 ), which can also be attributed to the fact that PPO is associated with phenolic metabolism in different plants, hence further affecting the fate of heavy metals in plant tissues. For example, PPO was involved in the polymerization of phenol that may trap and immobilize Cd by forming Cd-Ca crystals and restricting it in special epidermal structures (Lavid et al., 2001a; Lavid et al., 2001b).

In plant tissues, phenolic compounds, especially simple phenols and tannins that present within symplast and apoplast, can efficiently scavenge ROS to protect the vulnerable membrane structures and maintain photosynthesis, biosynthesis of proteins, and other metabolisms (Wang et al., 2014; Jiang et al., 2017). Numerous groups of phenolic compounds are united by a common path of biosynthesis, and therefore their content varies interconnected. Changes in the metabolism of phenols are the most important mechanism for plant adaptation to different stresses (Naikoo et al., 2019; Sharma et al., 2019). In mangrove plants like Aegiceras corniculatum, total phenolics and tannins concentration markedly increased with increasing Cd stress indicating that phenolic compounds play an important role in responding to Cd stress and act as antioxidants (Guangqiu et al., 2007). This was consistent with the current study that Cd stress generally increased the concentration of total phenolics and tannins in A. marina ( Figure 6 ). Simultaneously, correlations between Cd level and phenolic compounds also suggested the effectiveness of phenolic compounds in the tolerance and detoxification of plants under Cd stress ( Figure 3 ). More importantly, tannins and other phenolic compounds have a strong ability to chelate heavy metals, which have profound effects on the bioavailability, translocation and accumulation of Cd (Wang et al., 2014). Lavid et al. (Lavid et al., 2001b) showed that soluble phenols and tannins can chelate heavy metal ions with hydroxyl and carboxyl function groups. Similarly, Jiang et al. (Jiang et al., 2017) evidenced that phenolic compounds mediated the fate of Cd in both symplast and apoplast. Phenolic compounds negatively affect the translocation of Cd through adsorption, chelation, etc., and transfer those complexes to the “inactive” cell walls and vacuoles to reduce the biotoxicity and restrict Cd translocation from roots to leaves. In this study, Cd₁ stress did not significantly impact the concentration of total phenolics and tannins, while Cd₂ caused a significant increase in phenolic compounds of different tissues ( Figure 6 ). This may be due to the accumulation of Cd under higher Cd stress reaching the threshold of inducing the response of phenolic metabolism-associated tolerance and detoxification systems. Similarly, in K. obovata, antioxidant enzymes were reported to be more sensitive and respond more rapidly than phenolic compounds (Yan and Tam, 2011). Notably, the increase of phenolic compounds in different tissues under Fe₁ and Fe₂ supply can be attributed to the moderate Fe supply promoted photosynthesis in which plants assimilate inorganic carbons and further enhanced the biosynthesis of phenolic compounds ( Figures 1 , 6 ). However, relative to Fe_2, a higher Fe₃ supply inhibited photosynthesis ( Figure 1 ), thus resulting in an equal or lower phenolic compounds concentration in different tissues ( Figure 6 ), again demonstrating that excess Fe supply could also be a stress factor. Interestingly, under Cd₂ stress, total phenolics in roots were not significantly affected by different Fe treatments ( Figure 6 ), this is probably because the synthesis of phenolic compounds in roots relied mainly on carbon allocation from leaves to roots, and under Cd₂ stress, the downward translocation of phenolic compounds and other organic matters were inhibited, due to heavy metal stress (Kosola et al., 2006).

There have been studies on Fe supply alleviating phytotoxicity induced by Cd stress in different plants (mainly on terrestrial plants and corps, Table 1 ). The mechanisms include promoting photosynthesis, regulating antioxidant systems, and directly or indirectly affecting the uptake and transportation of metal ions, thus maintaining intracellular homeostasis and plant growth under Cd stress. However, there are few similar studies on intertidal zone ecosystems and coastal wetland plants, particularly mangroves, and focus on the activities of FCR, which play an unreplaceable role in Fe uptake by strategy I plant species. Intertidal zones are critical transition areas between the terrestrial and marine ecosystems. Unlike the “relatively stable” terrestrial habitats, numerous unique biogeochemical cycles of different nutrient elements and heavy metals occur or operate at different levels in the intertidal zone, a “crossroads” for the flow and exchange of materials (Zhou et al., 2011; Thomas et al., 2014; Jian et al., 2017b; Hong et al., 2021b). This could be attributed to the alternate cycles between aerobic and anaerobic conditions in sediments caused by intermittent tidal inundation (Wu et al., 2022b). In addition to controlling the mineralization of organic matter and the speciation, transformation, and migration of heavy metals, the natural tidal also deeply affected the speciation and bioavailability of Fe and contributed to the limitation of bioavailable Fe in the intertidal zone (Alongi, 2010). Simultaneously, as a prominent form of permanent pollutants, heavy metals are one of the notable threats to mangroves that connect and mediate a range of biotic and abiotic processes in intertidal habitats (Gao et al., 2016; Steinmuller et al., 2020; Wu et al., 2022b). Furthermore, the limitation of bioavailable Fe in sediments may further exacerbate the threat of heavy metal contamination to mangroves (Jian et al., 2019). The current study suggested that in the Fe-limited intertidal zones, for mangrove plants, in addition to mediating and regulating plants’ tolerance and detoxification mechanisms through the above pathways, Fe supply also regulates phenolic metabolism that played an irreplaceable role in fixing heavy metals and antioxidation (Yan and Tam, 2011; Wang et al., 2014). Simultaneously, the Cd translocation factor tended to decrease with increasing phenolic compound concentrations in different tissues. Therefore, Fe-regulated phenolic metabolism and other mechanisms are key factors in decelerating the translocation of Cd, decreasing damage caused by Cd toxicity, and maintaining the growth of A. marina under Cd stress. Moreover, FCR serves as the core component/mechanism of the Fe uptake by mangroves. When exposed to Cd stress, the increased FCR activity, along with the application of a moderate amount of Fe, could enhance the assimilation of Fe by plant tissues. This, in turn, enhances the detoxification mechanisms mentioned above, alleviates Cd toxicity, and ultimately improves the growth of A. marina. Thus, this process may establish “positive feedback” and emphasize the important role of FCR in the uptake of Fe by plants.