Abstract
Magnesium nutrition is often forgotten, while its absence adversely affects numerous functions in plants. Magnesium deficiency is a growing concern for crop production frequently observed in lateritic and leached acid soils. Competition with other cations (Ca2+, Na+, and K+) is also found to be an essential factor, inducing magnesium deficiency in plants. This nutrient is required for chlorophyll formation and plays a key role in photosynthetic activity. Moreover, it is involved in carbohydrate transport from source-to-sink organs. Hence, sugar accumulation in leaves that results from the impairment of their transport in phloem is considered as an early response to Mg deficiency. The most visible effect is often recorded in root growth, resulting in a significant reduction of root/shoot ratio. Carbohydrate accumulation in source leaves is attributed to the unique chemical proprieties of magnesium. As magnesium is a nutrient with high mobility in plants, it is preferentially transported to source leaves to prevent severe declines in photosynthetic activity. In addition, Mg is involved in the source-to-sink transport of carbohydrates. Hence, an inverse relationship between Mg shortage and sugar accumulation in leaves is often observed. We hereby review all these aspects with a special emphasis on the role of Mg in photosynthesis and the structural and functional effects of its deficiency on the photosynthetic apparatus.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Magnesium (Mg) is a macronutrient often forgotten in crop production (Cakmak and Yazici 2010). In the last decades, several studies examined the relationship between Mg nutrition and plant growth in a number of higher plants (Fischer and Bremer 1993; Cakmak et al. 1994a; Fischer et al. 1998; Hermans et al. 2004, 2005; Hermans and Verbruggen 2005). Authors were more interested in its deficiency than in its toxicity, which was explained by a difficulty to detect toxicity symptoms even with high concentrations (Shaul et al. 1999). Hawkesford et al. (2012) attributed this shortage in toxicity reports to a great capacity of the vacuole to store magnesium within plant cells.
Despite the well-known number of functions attributed to magnesium, its deficiency in soils is a growing concern for high-productivity agriculture (Cakmak and Yazici 2010). This problem is common in soils fertilized only with N, P, and K, which may prevent Mg uptake. Similar antagonistic effect was also noticed in the presence of other competing cations, such as Ca2+, H+, NH4 +, and Al3+. Magnesium deficiency was found as well to be a critical concern in lateritic and leached sandy acid soils due to its potential for leaching (Mengel and Kirkby 2001; Shaul 2002; Cakmak and Yazici 2010; Gransee and Führs 2013). Its symptoms appear as leaf interveinal chlorosis with a development of chlorotic and necrotic lesions in later stages (Marschner and Cakmak 1989; Cakmak and Marschner 1992; Cakmak and Kirkby 2008). The main targets of Mg deficiency are photosynthesis and sugar transport from source-to-sink organs. In this work, we review Mg nutrition and deficiency in plants with a special emphasis on photosynthesis and carbohydrate partitioning.
Magnesium in the soil
Sprengel (1828) affirmed that “…when a plant needs 12 substances to develop, it will not grow if any one of these is not available in a sufficiently large amount as required by the nature of plants”. According to Maguire and Cowan (2002), Mg is the eighth most abundant mineral element on earth. The source rock material from which it originates is that containing different types of silicates, and magnesium contents depend on silicate types (muscovite > biotite > hornblende > augite > olivine). As compared to other cations (Ca2+, K+, and NH4 +), Mg2+ is relatively mobile in soils. The importance of magnesium derives from its chemical properties (size, charge, density, and structure) that make it unique amongst biological cations (Kehres and Maguire 2002). It is characterized by a high hydrated radius and sorbs weakly to soil colloids. It is therefore prone to leaching, mainly in acidic soil with low cation exchange capacity (Aitken et al. 1999; Grzebisz 2011), being the most important factor in decreasing Mg2+ availability for roots (Hermans et al. 2004). The effects of cation competition (Ca2+, K+, and Na+) were also found to significantly reduce Mg2+ availability (Broadley and White 2010). This scarcity can be accentuated with N, P, and K fertilizers without simultaneous Mg fertilization (Verbruggen and Hermans 2013). In summary, two reasons can explain magnesium deficiency: absolute deficiency and cation competition. Absolute deficiency is due to: (1) Mg contents in source rocks (Papenfuß and Schlichting 1979) and (2) Mg mobilization and leaching (Schachtschabel 1954; Grzebisz 2011). Cation competition can be natural or induced by the abusive use of fertilizers (Cakmak and Yazici 2010); it strongly inhibits Mg uptake by nutrient imbalances (Gransee and Führs 2013). Abiotic stress conditions, such as drought and heat, can severely aggravate Mg deficiency by the inhibition of its uptake, since it is transported by mass flow (Gransee and Führs 2013). By contrast, Cakmak and Yazici (2010) stated specific benefits of Mg in the protection of soils from Al toxicity. Indeed, it was reported that magnesium can play an important role in alleviating Al toxicity in acid soils with only micromolar levels in comparison with Ca that is needed in millimolar concentrations (Silva et al. 2001).
Magnesium roles in plants
Magnesium is an essential macronutrient for the plant growth and development (Gransee and Führs 2013) and numerous key functions in plants (Cakmak and Yazici 2010). Its strong electrophilic axial coordination due to its tendency to form octahedral complexes enables it to occupy the central position in chlorophyll molecule (Beale 1999). Mg is also a phloem-mobile nutrient and its remobilization occurs from older leaves to younger ones (Taiz and Zeiger 2010). According to Cakmak and Yazici (2010), up to 35 % of the total Mg content in plants is located in chloroplasts, and the fraction remove of Mg pool directly associated with chlorophyll molecules constitutes 15–20 % of the total leaf content (Mengel and Kirkby 1987; Wilkinson et al. 1990). The remaining fraction (80–85 %) is present in mobile forms (Marschner 2012), which may explain the importance of Mg in photosynthate export. According to Cakmak and Yazici (2010), the importance of magnesium in phloem loading is related to its interaction with ATP fuelling; the H+-ATPase enzyme which provides energy for phloem loading process and maintains sucrose transport into phloem cells.
Mg is considered as a cofactor and allosteric modulator for more than 300 enzymes, including carboxylases, phosphatases, kinases, RNA polymerases, and ATPases. It also plays in important role in chelation with nucleotide tri- and di-phosphate forms (Pakrasi et al. 2001; Cowan 2002; Shaul 2002; Hawkesford et al. 2012), in addition to its involvement in the electron transport chain in chloroplasts (Ding et al. 2006). It is also known that magnesium has an essential role in cell energy balance due to its interaction with various metabolites, mainly nucleoside tri- and di-phosphates (Igamberdiev and Kleczkowski 2003). Cakmak and Yazici (2010) reported that Mg is involved in some other functions, such as protein synthesis and reactive oxygen species (ROS) generation. The importance of Mg in grana stacking was reported by Kaftan et al. (2002), and LHCII was found to participate in that cation-mediated formation of grana apart of being the major antenna for PSII (Hermans et al. 2004).
Mg stresses in plants
Mg concentrations in soil solutions are generally considered between 125 μM and 8.5 mM (Niu et al. 2014). Their variation is related to different factors: texture and cation exchange capacity of the soil (Hariadi and Shabala 2004), water availability, competing cation concentration, crop cultivation, and fertilizer regime (Broadley et al. 2008; Mikkelsen 2010). Hence, below 125-μM Mg plants may be subjected to Mg deficiency, while above 8.5 mM, they may face toxic effects that impair their growth and development (Guo et al. 2015). According to Tisdale et al. (1993), magnesium concentration in soil solution is typically between 0.2 and 2 mM in many soils of temperate regions. However, under some environmental conditions, many species (pasture, maize, potato, sugar beet…) can suffer from Mg deficiency even at these levels of available magnesium (Tan et al.1991; Tisdale et al. 1993; Hailes et al. 1997; Aitken et al. 1999).
Mg toxicity
Mg toxicity is a common problem in serpentine soils formed by the weathering of ultramafic rocks, such as in California (Brady et al. 2005) and Serbia areas (Vicić et al. 2014). These soils are known by macronutrient deficiencies (Ca, N, P, K), macronutrient toxicity (extremely high Mg:Ca ratio), and micronutrient toxicity (Mn, Fe, Ni…). Only serpentine-tolerant plants are able to survive in such high Mg conditions (Gao et al. 2015). To cope with Mg toxicity and avoid Ca deficiency, serpentine-tolerant plants have developed several physiological adaptations, including: (1) vacuole capacity to store excessive magnesium (Stelzer et al. 1990), (2) selective Ca uptake at the root and translocation to shoot levels, (3) restriction of internal Mg accumulation, and (4) Mg exclusion or sequestration at the root level (Alexander et al. 2007; Turner et al. 2010; O’Dell and Rajakaruna 2011).
Mg deficiency
Causes
Low Mg concentration in the soil
Highly weathered, acidic, and sandy soils are known to be Mg-deficient soils, since this nutrient is subjected to leaching in considerable amounts. Many findings were in accordance to indicate that magnesium is highly leached in these soils. According to Gransee and Führs (2013), magnesium leaching can reach up 25 kg ha−1, while Mesić et al. (2007) explained that depending on many factors (crop type, drainage volume…), this value can be higher (45–70 kg ha−1) in soils with limited fertility.
Calcareous soils
The presence of calcium and bicarbonate (HCO3 −) with high amounts in calcareous soils is known to prevent Mg uptake by competing effect, resulting in magnesium depletion (Cakmak and kirkby 2008; Gransee and Führs 2013; Farhat et al. 2015b). It was also found that the formation of MgCO3 in alkaline soils reduces Mg availability to plants (Broadley and White 2010).
Mg competition with Ca and K
It is well known that under Ca, Mg, or K deficiency, a relative or an absolute excess of the other cations can occur (Bergmann 1992). Indeed, these nutrients are strongly antagonistic and Mg is the least taken up nutrient (Voogt 1998). This poor ability of roots to take up Mg is attributed not only to root tissues but also to other plant organs (Mengel and Kirkby 2001). Schimanski (1981) supported these observations and reported that Mg availability can strongly modify Ca or K uptake, while Mg translocation can be restricted from roots to shoots by K and Ca. This phenomenon was observed in sunflower plants grown under insufficient Mg supply that showed an enhancement of Ca and K uptake (Lasa et al. 2000). Similar results were found by Hermans et al. (2004) who noticed in Mg-deficient sugar beet, a marked increase of calcium in roots and petioles and of potassium in all plant parts. These observations were in accordance to confirm the hypothesis of Peuke et al. (2002) who reported that a deficient nutrient enhances the uptake of other ones to compensate the charge balance of the omitted ion. In leaf mesophyll cells of bean plants, Mg uptake is facilitated by two systems: a non-selective ion channel that can transport calcium and potassium in both leaves and roots, resulting in an increase of their concentrations, while under Mg depletion conditions, another system (H+/Mg2+ exchanger) is used (Hariadi and Shabala 2004). Hence, the competition for uptake was considered as a consequence of the lack of specificity of the individual uptake systems for each cation (Shaul 2002; Gardner 2003; Deng et al. 2006; Marschner 2012). This antagonistic effect was often observed in the presence of Mg, while a synergistic one was revealed by Narwal et al. (1985) and Ding et al. (2006) in the absence of Mg.
Antagonistic effects
In rice plants subjected to increased K concentrations; both Mg concentrations and uptake were found to be reduced significantly in leaves and roots. However, no effect on Mg concentrations was reported under low K supply, which suggests that the antagonistic effect of K on Mg uptake was more marked than that of Mg on K uptake (Ding et al. 2006). These authors explained such results by a restriction of Mg translocation from roots to shoots. Farhat et al. (2013) noticed similar effects in safflower plants treated with excessive KCl concentration (60 mM KCl) that showed a significant decrease in Mg and Ca concentrations in all plant parts. This decrease was more pronounced in the case of magnesium under combined effects of high KCl concentration and low Mg supply (0.01 mM Mg). By contrast, no effect on potassium concentrations was noticed under Mg deficiency. According to Maguire and Cowan (2002), magnesium requires ion-specific proteins due to its specific characteristics. Thus, Mg has an ionic radius smaller than that of K while its hydrated radius is bigger. Another difference was found in the mechanisms involved in the transport of these two nutrients to roots (mass flow versus diffusion), resulting in a significant difference between K and Mg concentrations in soil solution mainly in the rhizosphere (Zhang and George 2002; Marschner 2012). In this context, Gransee and Führs (2013) reported that unspecific Mg transporters can be blocked by a high K availability in the soil/rhizosphere. For K uptake, two mechanisms were suggested: a “High-Affinity Transport System” (HATS) was proposed for a limited K concentration range, while a “Low-Affinity Transport System” (LATS) was suggested for over wide K concentration range (Britto and Kronzucker 2008).
Synergistic effects
These effects were noticed by Ding et al. (2006) between K+ and Mg2+ ions in rice plants. These authors found that Mg supply improved biomass yield and photosynthesis rate in rice plants fed with low K concentrations. However, no correction was noticed in chlorophyll concentrations. This supply of Mg was associated with an enhancement of K uptake and translocation from roots to shoots. The authors supposed that Mg could substitute K in some of its functions, which supports the hypothesis given by Bedi and Sekhon (1977) who suggested that some functions can be accomplished by one cation (Ca2+, K+, or Mg2+) in the absence of another.
Symptoms
Being a key constituent of chlorophyll molecule, magnesium is associated with leaf yellowing in the form of interveinal chlorosis in older leaves under Mg-deficiency stress (Cakmak and Yazici 2010). The appearance of these symptoms is explained by the high involvement of magnesium in the synthesis of chlorophylls, the main pigments responsible for light harvesting in plants. Hence, magnesium depletion results in photosynthesis inhibition, carbohydrate accumulation in source leaves, and, consequently, in root growth reduction (Cakmak et al. 1994a, b), as well as in alterations in chloroplast ultrastructure (Fink 1993; Puech and Mehne-Jakobs 1997). The main aspects of Mg deficiency in plants reviewed in this study were summarized in Fig. 1. According to Paul and Foyer (2001), the disruption of carbohydrate balance between source and sink organs may accelerate leaf senescence due to an alteration of magnesium chelatase, an important enzyme responsible for inserting Mg into protoporphyrin IX, as the first step of chlorophyll biosynthesis (Walker and Weinstein 1991). An accumulation of protoporphyrin IX due to the alteration of magnesium chelatase may enhance the chlorosis development (Cakmak and Kirkby 2008), inducing an over-reduction of the photosynthetic electron transport and an over-production of ROS (Hermans et al. 2005; Cakmak and Kirkby 2008).
As recorded in many species, the exposure of Sulla carnosa plants to Mg-free medium (0 mM Mg) or low Mg concentrations (0.01 mM Mg) resulted in typical interveinal chlorotic areas affecting at a first step old leaves then progressing towards the younger ones and developing later into necrotic spots (Farhat et al. 2014). These observations were reported in a number of plant species grown under low Mg bioavailability, such as: Arabidopsis thaliana (Hermans and Verbruggen 2005) and sugar beet plants (Hermans et al. 2004). It was established that the appearance of Mg-deficiency symptoms is highly related to light intensity. Hence, high light intensity was found to increase the development of interveinal chlorosis due to an enhancement of damaging highly ROS generation in chloroplasts. Marschner and Cakmak (1989) found that the exposure of bean plants to high light intensity under sufficient Mg supply or to low light intensity (80 mmol photons m−2 s−1) under Mg-deficiency conditions did not induce leaf chlorosis. By contrast, they noticed that Mg-deficient plants exposed to high light intensity (480 mmol photons m−2 s−1) rapidly showed leaf chlorosis. According to these authors, such an aggravation of chlorosis by high light was not due to a decrease of Mg concentrations in leaves, but to a direct involvement of photooxidative destruction of chlorophyll and membrane lipids. Foyer and Noctor (2005) affirmed that magnesium deficiency may involve a programmed cell damage related to oxidative damage in chloroplasts. A similar effect was noticed with heat stress on Mg-deficient plants that were sensitive to high temperatures. Hence, wheat and maize plants exhibited interveinal chlorosis on their older leaves as grown under low Mg supply at 25 °C, and the effect was aggravated at 35 °C (Mengutay et al. 2013).
Photosynthetic activity alteration by Mg deficiency
Magnesium deficiency was found to adversely affect ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) involved in CO2 fixation (Andersson 2008), which may explain the reduction of photosynthesis rate (Fischer 1997; Sun and Payn 1999; Ridolfi and Garrec 2000; Hermans and Verbruggen 2005). The inhibitory effect of magnesium deprivation on photosynthetic capacity and net CO2 assimilation was noticed in several plant species (Terry and Ulrich 1974; Fischer 1997; Sun and Payn 1999; Laing et al. 2000; Sun et al. 2001; Ridolfi and Garrec 2000; Hariadi and Shabala 2004; Hermans and Verbruggen 2005; Ling et al. 2009; Yang et al. 2012; Farhat et al. 2015a).
According to Ling et al. (2009), non-stomatal limitations might be the major factors determining the response of photosynthesis to Mg deficiency, since lower CO2 assimilation is accompanied by an increase in intercellular CO2 concentration. Indeed, Mg deficiency has been shown to induce an impairment of the linear photosynthetic electron transport (Hermans et al. 2004; Hermans and Verbruggen 2005; Tang et al. 2012; Farhat et al. 2015a), and this was suggested as the main factor contributing to decreased CO2 assimilation (Tang et al. 2012; Yang et al. 2012). Under magnesium deficiency, the structure and the partial photochemical activities of PSI and PSII were found to be affected in some species. Hence, a decrease of Fv/Fm ratio (maximum quantum efficiency of PSII) was noticed in Pinus radiata (Laing et al. 2000), Vicia faba (Hariadi and Shabala 2004), and Citrus seedlings (Yang et al. 2012) under Mg-deficiency conditions. However, in Mg-deficient Helianthus annuus plants, this parameter (Fv/Fm) and other fluorescence parameters were not affected (Lasa et al. 2000). A reduction of Fv/Fm was also reported in S. carnosa plants grown at 0 mM Mg (data not shown). Similar results were found by Hermans et al. (2004) in sugar beet plants. These authors suggested that the decline of PSII activity is due to a loss of PSII antenna or, alternatively, to a change in photosystem stoichiometry in favor of photosystem I (PSI), resulting in an enhanced chlorophyll a/chlorophyll b ratio. Hence, an increase in chlorophyll a/chlorophyll b ratio is frequently observed under Mg shortage conditions (Lavon et al. 1999; Balakrishnan et al. 2001; Hermans and Verbruggen 2005). However, in some cases, this ratio was found to be decreased (Ayala-Silva and Beyl 2005) or unaffected (Ceppi et al. 2012). The reduction in LHCII amounts in Mg-deficient Arabidopsis thaliana leaves corresponds to a disorganization of thylakoid membranes (Hermans et al. 2004).
The measurements of the oxidation state of P700 (P700+) (Klughammer and Schreiber 1991; Ivanov et al. 1998, 2006, 2012) in Mg-deficient leaves of S. carnosa showed a decline in the relative amount of oxidizable P700 (P700+), which was concomitant with a marked reduction in the abundance of the antenna (Lhca1 and Lhca2) and core (PsaA and PsaB) polypeptides of PSI reaction centre (Farhat et al. 2015a). Hermans et al. (2004) explained such decrease in the total oxidizable P700 pool of Mg-deficient sugar beet plants by a loss of PSI centres, affecting the electron transport rate. A similar effect was observed in spinach plants subjected to combined deficiencies of Mg and S with a more reduced plastoquinone (PQ) pool (Godde and Dannehl 1994; Dannehl et al. 1996).
Photooxidative damage, ultrastructure alteration, and antioxidant responses to Mg deficiency
The appearance of chlorosis and necrosis is considered as a symptom of damages in chloroplast ultrastructure. This hypothesis was confirmed in several plant species by transmission electron microscopy. Chloroplasts become round and bigger due to an accumulation of oversized starch grains with disrupted thylakoids (Fink 1993; Puech and Mehne-Jakobs 1997; Farhat et al. 2014). Thus, a relationship between carbohydrate accumulation and leaf chlorosis appearance was often suggested. Wingler et al. (2005) explained chlorosis progression by a reduction electron transport under magnesium deprivation, which impairs CO2 fixation and induces ROS generation. These species can seriously damage cell components, such as membrane lipids, proteins, and nucleic acids, resulting in metabolism disruption (Scandalios 2005). Malonyldialdehyde (MDA) accumulation was reported in Mentha pulegium (Candan and Tarhan 2003), Zea mays (Tewari et al. 2004), rice (Ding et al. 2008), and S. carnosa (Farhat et al. 2015b) plants as a general indicator of lipid peroxidation under low Mg availability conditions. However, it was established that under such conditions, the antioxidative defense system is stimulated to scavenge ROS that cause oxidative damages (Cakmak and Marschner 1992; Tewari et al. 2004, 2006; Riga et al. 2005; Yang et al. 2012). Hence, an induction of superoxide dismutase (SOD) activity was reported in various Mg-deficient plants, such as common bean (Cakmak and Marschner 1992), rice (Ding et al. 2008), and mulberry (Tewari et al. 2006), suggesting that under Mg deficiency, cells enhance their antioxidative defense system by initially increasing their SOD activities, since SOD is known to be the first enzyme involved in the protection of cells from the peroxidative attack of ROS (Bowler et al. 1992). The activities of other enzymes, such as catalase (CAT) and peroxidase (POD), may also be enhanced under such conditions. POD activity increase is explained by its high implication in the decomposition of H2O2 generated by SOD (Ding et al. 2008). This finding was concomitant with that found by Candan and Tarhan (2003) and Tewari et al. (2004, 2006) in Mg-deficient plants. However, it was noticed that CAT activity can decrease or remain constant in some cases (Tewari et al. 2004, 2006), indicating that severe deficiency could destroy the antioxidant system in plants. Kanazawa et al. (2000) found that a decline in SOD, CAT, and POD activities may also determine the sensitivity of plants to lipid peroxidation. Hence, when ROS production overcomes scavenging systems, the latter cannot provide a sufficient protection to membranes against photooxidation and oxidative stress occurs, resulting in a significant increase in MDA level (Ding et al. 2008).
Carbohydrate allocation disruption by Mg deficiency
In the majority of higher plants, the principal end products of leaf photosynthesis are starch and sucrose. Mineral deficiencies were supposed to affect carbohydrate partitioning (Ding and Xu 2011). The relationship between sugar partitioning and magnesium deficiency was studied by several authors (Hermans and Verbruggen 2005; Hermans et al. 2005; Cakmak et al. 1994a, b), who noticed that the most destructive effect of magnesium deficiency is sugar accumulation in source leaves, affecting later plant growth, photosynthetic activity, and leaf morphology. Thus, an accumulation of carbohydrates in source leaves and a reduction of root growth are considered as an earlier response to Mg deficiency, since it is involved in biomass formation and carbohydrate partitioning. In fact, carbohydrate accumulation together with the reduction of root/shoot ratio was reported in a variety of species under insufficient magnesium supply (Fischer and Bremer 1993; Cakmak et al. 1994a, b; Fischer et al. 1998; Mengutay et al. 2013). For this reason, chlorosis is not considered as suitable tool for an early diagnosis of Mg deficiency (Cakmak et al. 1994a, b; Ding et al. 2006), but as a late visible symptom (Gransee and Führs 2013). Farhat et al. (2014) observed a significant accumulation of soluble sugars (glucose, fructose, and sucrose) and starch in leaves of S. carnosa plants grown under absolute Mg deficiency (0 mM Mg) as well as under low magnesium availability (0.01 mM Mg), which correspond to the lowest pigment (Chla and Chlb) concentrations. Ericsson and Kahr (1995) considered that sucrose accumulation seems to be the major growth constraint, especially for roots. Cakmak et al. (1994a, b) associated this increase of carbohydrates in Phaseolus vulgaris plants to a sensitivity of phloem sucrose loading under magnesium limitations. Sucrose and starch accumulation was also noticed in rosette leaves of sugar beet plants fed with deficient magnesium nutrient solution. This accumulation was accompanied by an impairment of their export from leaves to roots and resulted in an imbalance between sucrose accumulation and its utilization (Hermans et al. 2005). Rook et al. (2001) attributed this accumulation to an antisense expression of sucrose symporters, while Zhao et al. (2000) explained it by a co-suppression of the plasma membrane H+-ATPase. According to some other authors (Ntsika and Deltrot 1986; Grusak et al. 1990; Paul and Foyer 2001), this increase is due to sink consumption reduction. Hence, being a mobile nutrient (80 % of magnesium is present in mobile forms), different hypotheses were given to explain the essential role of Mg in photosynthate export: (1) a structural damage and a destabilization in phloem tissue (Hannick et al. 1993), (2) a perturbation in the activity of sink organs, or (3) an impairment in phloem loading (Cakmak et al. 1994b; Hermans et al. 2005, 2006; Hermans and Verbruggen 2005). Cakmak and Kirkby (2008) reported that the third possibility may be related to a reduction of photosynthesis in Mg-deficient leaves. However, photosynthesis rate was found to be affected at later stages of this mineral deficiency. Thus, Mg starvation seems to have a direct functional and/or structural effect(s) on the phloem loading process of sucrose, confirming that photosynthesis alteration is not a sensitive indicator of Mg deficiency (Peaslee and Moss 1966). The importance of Mg in sucrose phloem loading was related to its interaction with nucleotidyl tri-phosphate (Mg2+-ATP) fuelling the H+-ATPases located in the plasma membranes of sieve tube cells. Therefore, under limited Mg concentrations, phloem loading inhibition into sink organs is explained by an impairment of H+/ATPase activity in phloem companion cells (Bush 1989; Zhao et al. 2000). In fact, the binding of Mg by ATP is disrupted, which reduces the level of Mg-ATP complexes required by plasma membrane-bound ATPases. This results in the inhibition of photosynthate export via phloem (Hanstein et al. 2011; White 2012).
Concluding remarks
Despite Mg involvement in several vital functions in plants, it is still “forgotten” at the fundamental and applied levels. At the fundamental level, many mechanisms, including Mg uptake, translocation, transport mechanisms, and proteins mediating its transport in plants need to be more elucidated. At the applied level, the problem of Mg deficiency should be avoided to improve crop production and quality through the implication of this nutrient in soil fertilization, in particular, in the case of combined effects of magnesium deficiency and other abiotic stresses, such as heat and high light that are known to accentuate Mg deprivation symptoms.
Author contribution statement
Nèjia Farhat prepared the manuscript, and Amine Elkhouni, Walid Zorrig, Abderrazak Smaoui, Chedly Abdelly, and Mokded Rabhi discussed and revised it.
References
Aitken RL, Dickson T, Hailes KJ, Moody PW (1999) Response of field-grown maize to applied magnesium in acidic soil in northeastern Australia. Aust J Agric Res 50:191–198
Alexander EB, Coleman RG, Keeler-Wolf T, Harrison S (2007) Serpentine geoecology of Western North America: geology, soils, and vegetation. Oxford University Press, New York
Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59:1555–1568
Ayala-Silva T, Beyl CA (2005) Changes in spectral reflectance of wheat leaves in response to specific macronutrient deficiency. Adv Space Res 2:305–317
Balakrishnan K, Rajendran C, Kulandaivelu G (2001) Differential responses of iron, magnesium, and zinc deficiency on pigment composition, nutrient content, and photosynthetic activity in tropical fruit crops. Photosynthetica 38:477–479
Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60:43–73
Bedi AS, Sekhon GS (1977) Effect of potassium and magnesium application to soils on the dry-matter yield and cation composition of maize. J Agric Sci 88:735–758
Bergmann W (1992) Nutritional disorders of plants-Development, visual and analytical diagnosis. Gustav Fischer Verlag, Germany
Bowler C, Montagu MV, Inz D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116
Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266
Britto DT, Kronzucker HJ (2008) Cellular mechanisms of potassium transport in plants. Physiol Plant 133:637–650
Broadley MR, White PJ (2010) Eats roots and leaves. Can edible horticultural crops address dietary calcium, magnesium and potassium deficiencies? Proc Nutr Soc 69:601–612
Broadley MR, Hammond JP, King GJ, Astley D, Bowen HC, Meacham MC et al (2008) Shoot calcium and magnesium concentrations differ between subtaxa, are highly heritable, and associate with potentially pleiotropic loci in Brassica oleracea. Plant Physiol 146:1707–1720
Bush DR (1989) Proton-coupled sucrose transport in plasmalemma vesicles isolated from sugar beet (Beta vulgaris L. cv. Great Western) leaves. Plant Physiol 89:1318–1323
Cakmak I, Kirkby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 133:692–704
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227
Cakmak I, Yazici AM (2010) Magnesium: a forgotten element in crop production. Better Crops 94:23–25
Cakmak I, Hengeler C, Marschner H (1994a) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45:1245–1250
Cakmak I, Hengeler C, Marschner H (1994b) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. J Exp Bot 45:1251–1257
Candan N, Tarhan L (2003) Relationship among chlorophyll-carotenoid content, antioxidant enzyme activities and lipid peroxidation levels by Mg2+ deficiency in the Mentha pulegium leaves. Plant Physiol Biochem 41:35–40
Ceppi MG, Oukarroum A, Nuran C, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant 144:277–288
Cowan JA (2002) Structural and catalytic chemistry of magnesium dependent enzymes. Biometals 15:225–235
Dannehl H, Wietoska H, Heckmann H, Godde D (1996) Changes in D1-protein turnover and recovery of photosystem II activity precede accumulation of chlorophyll in plants after release from mineral stress. Planta 199:34–42
Deng W, Luo K, Li D, Zheng X, Wei X, Smith W, Thammina C, Lu L, Li Y, Pei Y (2006) Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance. J Exp Bot 57:4235–4243
Ding Y, Xu G (2011) Low magnesium with high potassium supply changes sugar partitioning and root growth pattern prior to visible magnesium deficiency in leaves of Rice (Oryza sativa L.). Am J Plant Sci 2:601–608
Ding Y, Luo W, Xu G (2006) Characterisation of magnesium nutrition and interaction of magnesium and potassium in rice. Ann Appl Biol 149:111–123
Ding Y, Chang C, Luo W, Wu Y, Ren X, Wang P, Xu G (2008) High potassium aggravates the oxidative stress induced by magnesium deficiency in rice leaves. Pedosphere 18:316–327
Ericsson T, Kahr M (1995) Growth and nutrition of birch seedlings at varied relative addition rates of magnesium. Tree Physiol 15:85–93
Farhat N, Rabhi M, Falleh H, Lengliz K, Smaoui A, Abdelly C, Lachaal M, Karray-Bouraoui N (2013) Interactive effects of excessive potassium and Mg deficiency on safflower. Acta Physiol Plant 35:2737–2745
Farhat N, Rabhi M, Krol M, Barhoumi Z, Ivanov AG, McCarthy A, Abdelly C, Smaoui A, Huner NPA (2014) Starch and sugar accumulation in Sulla carnosa leaves upon Mg2+ starvation. Acta Physiol Plant. doi:10.1007/s11738-014-1592-y
Farhat N, Ivanov AG, Krol M, Rabhi M, Smaoui A, Abdelly C, Hüner NPA (2015a) Preferential damaging effects of limited magnesium bioavailability on photosystem I in Sulla carnosa plants. Planta. doi:10.1007/s00425-015-2248-x
Farhat N, Sassi H, Zorrig W, Abdelly C, Barhoumi Z, Smaoui A, Rabhi M (2015b) Is excessive Ca the main factor responsible for Mg deficiency in Sulla carnosa on calcareous soils? J Soil Sediment. doi:10.1007/s11368-015-1101-y
Fink S (1993) Microscopic criteria for the diagnosis of abiotic injuries to conifer needles. In: Huettl RF, Mueller-Dombois D (eds) Forest decline in the Atlantic and Pacific region. Springer, Berlin, pp 175–189
Fischer ES (1997) Photosynthetic irradiance curves of Phaseolus vulgaris under moderate or severe magnesium deficiency. Photosynthetica 33:385–390
Fischer ES, Bremer E (1993) Influence of magnesium deficiency on rates of leaf expansion, starch and sucrose accumulation and net assimilation in Phaseolus vulgaris. Physiol Plantarum 89:271–276
Fischer ES, Lohaus G, Heineke D, Heldt HW (1998) Magnesium deficiency resulted in accumulation of carbohydrates and amino acids in source and sink leaves of spinach. Physiol Plantarum 102:16–20
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signalling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875
Gao C, Zhao Q, Jianga L (2015) Vacuoles protect plants from high magnesium stress. PNAS 112:2931–2932
Gardner RC (2003) Genes for magnesium transport. Curr Opin Plant Biol 6:263–267
Godde D, Dannehl H (1994) Stress-induced chlorosis and increase in D1-protein turnover precede photoinhibition in spinach suffering under magnesium/sulphur deficiency. Planta 195:291–300
Gransee A, Führs H (2013) Magnesium mobility in soils as a challenge for soil and plant analysis, magnesium fertilization and root uptake under adverse growth conditions. Plant Soil 368:5–21
Grusak MA, Deltrot S, Ntsika G (1990) Short-term effect of heat-girdles on source leaves of Vicia faba. J Exp Bot 41:1371–1377
Grzebisz W (2011) Magnesium-food and human health. J Elem 16:299–323
Guo W, Chen S, Hussain N, Cong Y, Liang Z, Chen K (2015) Magnesium stress signaling in plant: just a beginning. Plant Signal Behav. doi:10.4161/15592324.2014.992287
Hailes KJ, Aitken RL, Menzies NW (1997) Magnesium in tropical and subtropical soils from north-eastern Australia. II. Response by glasshouse-grown maize to applied magnesium. Aust J Soil Res 35:629–641
Hannick AF, Waterkeyn L, Weissen F, van Prag HJ (1993) Vascular tissue anatomy of Norway spruce needles and twigs in relation to magnesium deficiency. Tree Physiol 13:337–349
Hanstein S, Wang XZ, Qian XQ, Friedhoff P, Fatima A, Shan YH, Feng K, Schubert S (2011) Changes in cytosolic Mg2+ levels can regulate the activity of the plasma membrane H+-ATPase in maize. Biochem J 435:93–101
Hariadi Y, Shabala S (2004) Screening broad beans (Vicia faba) for magnesium deficiency. II. Photosynthetic performance and leaf bioelectrical responses. Funct Plant Biol 31:539–549
Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Skrumsager Møller I, White P (2012) Functions of macronutrients. In: Marschner P (ed) Mineral nutrition of higher plants. Elsevier, Amsterdam, pp 135–189
Hermans C, Verbruggen N (2005) Physiological characterization of Mg deficiency in Arabidopsis thaliana. J Exp Bot 418:2153–2161
Hermans C, Jhonson GN, Strasser RJ, Verbruggen N (2004) Physiological characterization of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II. Planta 220:344–355
Hermans C, Bourgis F, Faucher M, Strasser RJ, Delrot S, Verbruggen N (2005) Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves. Planta 220:541–549
Igamberdiev AU, Kleczkowski LA (2003) Membrane potential, adenylate levels and Mg2+ are interconnected via adenylate kinase equilibrium in plant cells. Biochim Biophys Acta 1607:111–119
Ivanov AG, Morgan R, Gray GR, Velitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292
Ivanov AG, Hendrickson L, Krol M, Selstam E, Öquist G, Hurry V, Huner NPA (2006) Digalactosyl-diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to photosystem I acceptor-side limitations. Plant Cell Physiol 47:1146–1157
Ivanov AG, Allakhverdiev SI, Huner NPA, Murata N (2012) Genetic decrease in fatty acid unsaturation of phosphatidylglycerol increased photoinhibition of photosystem I at low temperature in tobacco leaves. Biochim Biophys Acta 1817:1374–1379
Kaftan D, Brumfeld V, Nevo R, Scherz A, Reich Z (2002) From chloroplasts to photosystems: in situ scanning force microscopy on intact thylakoid membranes. EMBO J 21:6246–6253
Kanazawa S, Sano S, Koshiba T, Ushimaru T (2000) Changes in antioxidative in cucumber cotyledons during natural senescence: comparison with those during dark-induced senescence. Physiol Plant 109:211–216
Kehres DG, Maguire ME (2002) Structure, properties and regulation of magnesium transport proteins. Biometals 15:261–270
Klughammer C, Schreiber U (1991) Analysis of light-induced absorbancy changes in the near-infrared spectral region. 1: characterization of various components in isolated chloroplasts. Z Naturforsch C 46:233–244
Laing W, Greer D, Sun O, Beets P, Lowe A, Payn T (2000) Physiological impacts of Mg deficiency in Pinus radiata: growth and photosynthesis. New Phytol 146:47–57
Lasa B, Frechilla S, Aleu M, González-Moro B, Lamsfus C, Aparicio-Tejo PM (2000) Effects of low and high levels of magnesium on the response of sunflower plants grown with ammonium and nitrate. Plant Soil 225:167–174
Lavon R, Salomon R, Goldschmidt EE (1999) Effect of potassium, magnesium, and calcium deficiencies on nitrogen constituents and chloroplast components in Citrus leaves. J Am Soc Hortic Sci 124:158–162
Ling LL, Peng LZ, Cao L, Jiang CL, Chun CP, Zhang GY, Wang ZX (2009) Effect of magnesium deficiency on photosynthesis characteristic of Beibei 447 Jinchen orange. J Fruit Sci 26:275–280
Maguire ME, Cowan JA (2002) Magnesium chemistry and biochemistry. Biometals 15:203–210
Marschner H (2012) In: Marschner P (ed) Mineral nutrition of higher plants. Academic Press, London
Marschner H, Cakmak I (1989) High light intensity enhances chlorosis and necrosis in leaves of zinc, potassium and magnesium deficient bean (Phaseolus vulgaris) plants. J Plant Physiol 134:308–315
Mengel K, Kirkby EA (1987) Principles of plant nutrition. International Potash Institute, Switzerland, pp 481–492
Mengel K, Kirkby EA (2001) Principles of plant nutrition. Kluwer Academic Publishers, Dordrecht
Mengutay M, Ceylan Y, Kutman UB, Cakmak I (2013) Adequate magnesium nutrition mitigates adverse effects of heat stress on maize and wheat. Plant Soil 368:57–72
Mesić M, Kisić I, Bašić F, Butorac A, Zgorelec Ž, Gašpar I (2007) Losses of Ca, Mg and SO4 2− with drainage water at fertilization with different nitrogen rates. Agric Conspec Sci 72:53–58
Mikkelsen R (2010) Soil and fertilizer magnesium. Better. Crops 94:26–28
Narwal RP, Kumar V, Singh JP (1985) Potassium and magnesium relationship in cowpea (Vigna unguiculata (L.) Walp.). Plant Soil 86:129–134
Niu Y, Chai R, Liu L, Jin G, Liu M, Tang C, Zhang Y (2014) Magnesium availability regulates the development of root hairs in Arabidopsis thaliana (L.) Heynh. Plant Cell Environ 37:2795–2813
Ntsika G, Deltrot S (1986) Changes in apoplastic and intracellular leaf sugars induced by the blocking of export in Vicia faba. Physiol Plant 68:145–153
O’Dell RE, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In: Harrison SP, Rajakaruna N (eds) Serpentine: evolution and ecology of a model system. University of California Press, Berkeley, pp 97–137
Pakrasi H, Ogawa T, Bhattacharrya-Pakrasi M (2001) Transport of metals: a key process in oxygenic photosynthesis. In: Aro EM, Anderson B (eds) Regulation of photosynthesis. Kluwer, Dordrecht, pp 253–264
Papenfuß KH, Schlichting E (1979) Bestimmende Faktoren des Mg-Haushaltes von Böden in der Bundesrepublik Deutschland. Magnes Bull 1:12–14
Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400
Peaslee DE, Moss DN (1966) Photosynthesis in K and Mg-deficient maize (Zea mays) leaves. Soil Sci Soc Am Proc 30:220–223
Peuke AD, Jeschke WD, Hartung W (2002) Flows of elements, ions and abscisic acid in Ricinus communis and site of nitrate reduction under potassium limitation. J Exp Bot 53:241–250
Puech L, Mehne-Jakobs B (1997) Histology of magnesium deficient Norway spruce needles influenced by nitrogen source. Tree Physiol 17:301–310
Ridolfi M, Garrec JP (2000) Consequences of an excess Al and a deficiency in Ca and Mg for stomatal functioning and net carbon assimilation of beech leaves. Ann Forest Sci 57:209–218
Riga P, Anza M, Garbisu C (2005) Suitability of the antioxidative system as marker of magnesium deficiency in Capsicum annuum L. plants under controlled conditions. Plant Growth Regul 46:51–59
Rook F, Corke F, Card Munz G, Smith C, Bevan MW (2001) Impaired sucrose induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signaling. Plant J 26:421–433
Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014
Schachtschabel P (1954) Das pflanzenverfügbare Magnesium des Bodens und seine Bestimmung. J Plant Nutr Soil Sci 67:9–23
Schimanski C (1981) The influence of certain experimental parameters on the flux characteristics of Mg-28 on the case of barely seedlings grown in hydroculture. Landwirtsch Forsch 34:154–165
Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309–323
Shaul O, Hilgemann DW, Almeida-Engler J, Van Montagu M, Inzé D, Galili G (1999) Cloning and characterization of a novel Mg2+/H+ exchanger. EMBO J 18:3973–3980
Silva IR, Smyth TJ, Carter TE, Rufty TW (2001) Altered aluminum root elongation inhibition in soybean genotypes in the presence of magnesium. Plant Soil 230:223–230
Sprengel C (1828) Von den Substanzen der Ackerkrume und des Untergrundes. Journal fur Tecnische und Okonomische Chemie 2:423–474
Stelzer R, Lehmann H, Krammer D, Luttge U (1990) X-Ray microprobe analysis of vacuoles of spruce needle mesophyll, endodermis and transfusion parenchyma cells at different seasons of the year. Bot Acta 103:415–423
Sun OJ, Payn TW (1999) Magnesium nutrition and photosynthesis in Pinus radiata: clonal variation and influence of potassium. Tree Physiol 19:535–540
Sun OJ, Gielen GTHP, Sands R, Smith CT, Thorn AJ (2001) Growth, Mg nutrition and photosynthetic activity in Pinus radiata: evidence that NaCl addition counteracts the impact of low Mg supply. Trees 15:335–340
Taiz L, Zeiger E (2010) Plant physiology. Sinauer Associates, Sunderland
Tan K, Keltjens WG, Findenegg R (1991) Role of magnesium in combination with liming in alleviating acid-soil stress with the aluminium-sensitive sorghum genotype CV323. Plant Soil 136:65–71
Tang N, Li Y, Chen LS (2012) Magnesium deficiency-induced impairment of photosynthesis in leaves of fruiting Citrus reticulata trees accompanied by up-regulation of antioxidant metabolism to avoid photo-oxidative damage. J Plant Nutr Soil Sci 175:784–793
Terry N, Ulrich A (1974) Effects of magnesium deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiol 54:379–381
Tewari RK, Kumar P, Tewari N, Srivastava S, Sharma PN (2004) Macronutrient deficiencies and differential antioxidant responses-influence on the activity and expression of superoxide dismutase in maize. Plant Sci 166:687–694
Tewari RK, Kumar P, Sharma PN (2006) Magnesium deficiency induced oxidative stress and antioxidant responses in mulberry plants. Sci Hort 108:7–14
Tisdale SL, Nelson WL, Beaton JD, Havlin JL (1993) Soil fertility and fertilisers. Prentice Hall, Upper Saddle River
Turner TL, Bourne EC, Von Wttberg EJ, Hu TT, Nuzhdin SV (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42:260–263
Verbruggen N, Hermans C (2013) Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant Soil 368:87–99
Vicić DD, Stoiljković MM, Bojat NČ, Sabovljević MS, Stevanović BM (2014) Physiological tolerance mechanisms of serpentine tolerant plants from Serbia. Rev Écol (Terre Vie) 69
Voogt W (1998) The growth of beefsteak tomato as affected by K/Ca ratios in the nutrient solution. Glasshouse Crops Research Station Naaldwijk, The Netherlands
Walker CJ, Weinstein JD (1991) Further characterization of the magnesium chelatase in isolated developing cucumber chloroplasts. Plant Physiol 95:1189–1196
White PJ (2012) Ion uptake mechanisms of individual cells and roots: short-distance transport. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Academic Press, London, pp 7–47
Wilkinson S, Welch R, Mayland H, Grunes D (1990) Magnesium in plants: uptake, distribution, function and utilization by man and animals. Metal Ions Biol Syst 26:33–56
Wingler A, Brownhill E, Pourtau N (2005) Mechanisms of the light-dependent induction of cell death in tobacco plants with delayed senescence. J Exp Bot 56:2897–2905
Yang GH, Yang LT, Jiang HX, Li Y, Wang P, Chen LS (2012) Physiological impacts of magnesium-deficiency in Citrus seedlings: photosynthesis, antioxidant system and carbohydrates. Trees 26:1237–1250
Zhang J, George E (2002) Changes in the extractability of cations (Ca, Mg and K) in the rhizosphere soil of Norway spruce (Picea abies) roots. Plant Soil 243:209–217
Zhao R, Dielen V, Kinet JM, Boutry M (2000) Cosupression of a plasma membrane H+-ATPase isoform impairs sucrose translocation, stomatal opening, plant growth and male fertility. Plant Cell 12:535–546
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A.K. Kononowicz.
Rights and permissions
About this article
Cite this article
Farhat, N., Elkhouni, A., Zorrig, W. et al. Effects of magnesium deficiency on photosynthesis and carbohydrate partitioning. Acta Physiol Plant 38, 145 (2016). https://doi.org/10.1007/s11738-016-2165-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2165-z