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First published online April 15, 2009; 10.1104/pp.108.134601 Plant Physiology 150:825-833 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Manganese Deficiency Leads to Genotype-Specific Changes in Fluorescence Induction Kinetics and State Transitions1,[C],[OA]Plant and Soil Science Laboratory, Department of Agriculture and Ecology (S.H., K.H.L., C.A.H., S.B.S., P.P.), and The Villum Kann Rasmussen Research Center "Pro-Active Plants," Department of Plant Biology and Biotechnology, Faculty of Life Sciences, University of Copenhagen, DK–1871 Frederiksberg C, Copenhagen, Denmark (A.H., P.E.J.)
Barley (Hordeum vulgare) genotypes display a marked difference in their ability to tolerate growth at low manganese (Mn) concentrations, a phenomenon designated as differential Mn efficiency. Induction of Mn deficiency in two genotypes differing in Mn efficiency led to a decline in the quantum yield efficiency for both, although faster in the Mn-inefficient genotype. Leaf tissue and thylakoid Mn concentrations were reduced under Mn deficiency, but no difference between genotypes was observed and no visual Mn deficiency symptoms were developed. Analysis of the fluorescence induction kinetics revealed that in addition to the usual O-J-I-P steps, clear K and D steps were developed in the Mn-inefficient genotype under Mn deficiency. These marked changes indicated damages to photosystem II (PSII). This was further substantiated by state transition measurements, indicating that the ability of plants to redistribute excitation energy was reduced. The percentage change in state transitions for control plants with normal Mn supply of both genotypes was 9% to 11%. However, in Mn-deficient leaves of the Mn-inefficient genotypes, state transitions were reduced to less than 1%, whereas no change was observed for the Mn-efficient genotypes. Immunoblotting and the chlorophyll a/b ratio confirmed that Mn deficiency in general resulted in a significant reduction in abundance of PSII reaction centers relative to the peripheral antenna. In addition, PSII appeared to be significantly more affected by Mn limitation than PSI. However, the striking genotypic differences observed in Mn-deficient plants, when analyzing state transitions and fluorescence induction kinetics, could not be correlated with specific changes in photosystem proteins. Thus, there is no simple linkage between protein expression and the differential reduction in state transition and fluorescence induction kinetics observed for the genotypes under Mn deficiency.
Manganese (Mn) deficiency is a major plant nutritional disorder, often caused by an alkaline soil pH, which favors oxidation of soluble Mn2+ to the plant-unavailable form MnO2. Mn-deficient crops are found in many areas of the world but are especially widespread in Australia, the United States, Asia, and northern Europe, including Scandinavia. A recent survey estimated that approximately 30% of soils in China are Mn deficient, causing severe yield and quality reductions in crops (Yang et al., 2007  ). Likewise, Mn deficiency has become the foremost plant nutritional problem in major parts of Scandinavia (Hebbern et al., 2005, 2009).
The oxygen-evolving complex (OEC) in PSII has a metalloenzyme core containing both Mn2+ and Ca2+ ions as well as the halogen ion Cl– (Kok et al., 1970
Genotypes of winter barley (Hordeum vulgare) are known to respond differently to low Mn availability (Hebbern et al., 2005 Despite the fact that Mn is a key component of PSII, there have not been any previous attempts to examine the relationship between differential Mn efficiency and the resistance of the photosynthetic apparatus to perturbations induced by Mn deficiency. Thus, this study was undertaken in order to identify genotypic differences in the energy transfer within the PSII reaction center that may correlate with Mn efficiency. The genotypic differences were investigated by pulse amplitude-modulated fluorescence, analysis of the fluorescence induction kinetics, and selected PSII and PSI components.
Plant Growth under Mn Deficiency
The development of visible leaf symptoms caused by Mn deficiency could be prevented if the quantum yield efficiency of PSII (Fv/Fm) on dark-adapted leaves was kept above 0.55 for a period of at least 4 weeks under the conditions given (data not shown). Thus, the intensity of Mn deficiency in plants was followed and controlled by measuring Fv/Fm throughout the experimental period (Fig. 1A
). Control plants were successfully maintained at Fv/Fm values close to the theoretical optimum of 0.83 (Björkman and Demmig, 1987
Mn Content in Leaf Tissue and Thylakoids
The Mn concentration was analyzed in the youngest fully expanded leaf 44 and 50 d after the induction of Mn deficiency (Fig. 2
), and the Mn concentration of thylakoids was analyzed prior to termination of the experiment. These results supported that the low Fv/Fm values were caused by Mn deficiency. The Mn concentration in the thylakoids of the inefficient genotype was reduced from 0.75 ± 0.03 to 0.48 ± 0.10 mg Mn g–1 Chl under Mn deficiency, whereas the similar values for the efficient line were a reduction from 0.88 ± 0.09 to 0.61 ± 0.02 mg Mn g–1 Chl. Thus, clearly less Mn was found in the thylakoids of Mn-deficient plants, but no significant difference was found between the genotypes. Likewise, the Mn concentrations in leaves from deficient plants were significantly below the critical threshold concentrations of 17 µg Mn g–1 dry weight for both barley genotypes (Reuter et al., 1997
Mn Deficiency Leads to the Development of K and D Steps in the Chl a Fluorescence Induction Curves
Besides reducing the Fv/Fm value, Mn deficiency introduced a number of distinct changes in the position of the O-J-I-P steps and the general shape of the Chl a fluorescence induction curves (Fig. 3
). When the degree of Mn deficiency intensified and the Fv/Fm value was reduced below 0.67, a new step at 0.2 to 0.4 ms appeared in the fluorescence induction curves, designated as the K step by Strasser et al. (2004)
State Transitions
Plants have the ability to adjust the energy input to PSII and PSI by moving a mobile pool of the light-harvesting complex (LHCII) proteins (Lhcb1, Lhcb2, and Lhcb3) between the photosystems by a state transition process. The mobility of LHCII between photosystems is controlled by phosphorylation (Bellafiore et al., 2005
In the control plants (Fig. 4A), the maximum fluorescence in state 1 (Fm1) was clearly higher than in state 2 (Fm2), indicating that the ability to adjust to PSI and PSII light was intact. The percentage change in state transitions [(Fm1 – Fm2)/Fm1] was measured to 9% to 11% in healthy control plants and was not significantly different between the control samples of both genotypes (Fig. 5A ). In Figure 4B, the effect of Mn deficiency on state transition in the Mn-inefficient genotype Antonia is illustrated, and it is clearly seen that the ability to perform state transitions has been reduced significantly. The percentage change in state transition for Mn-deficient leaves was reduced to less than 1% of the Mn-inefficient genotype Antonia, whereas Mn deficiency did not cause any significant effect on state transitions in the Mn-efficient genotype Vanessa (Fig. 5A).
The Fv/Fm was determined immediately before the state transition experiments, and despite a striking difference in the ability to perform state transitions, at both 38 and 50 d after Mn deficiency induction, no significant differences in Fv/Fm values between Mn-deficient Vanessa and Antonia were observed on both occasions (Fig. 1A). Immunoblotting showed that there was no significant difference in the amount of Lhcb1 between control and Mn-deficient leaves, but a marked decrease in the phosphorylated form of LHCII (P-Lhcb1 and P-Lhcb2) was observed when plants were exposed to Mn deficiency (Fig. 5B). Likewise, a significant reduction in the Chl a concentration was observed in Mn-deficient plants, whereas the Chl b concentration remained stable (Fig. 5C). The Chl measurements suggest a significant reduction in the amount of functional PSII reaction centers relative to the peripheral antenna under Mn deficiency, which subsequently was confirmed by the immunoblot-based quantification of PsbA (Fig. 5D). Generally, Mn deficiency led to a 75% reduction in the amount of PsbA (representing PSII), whereas PSI-F (representing PSI) under the same conditions was reduced to approximately 45% in both genotypes. Time of analysis is a very important parameter to consider when nutrient deficiency studies are undertaken, as the impact of the physiological perturbations change with age and intensity of the deficiency. However, those trends described above were found to be highly consistent and were confirmed by repeating parts of the experiments several times using plants of different physiological age and severity of Mn deficiency (data not shown). Thus, Mn deficiency resulted in a clear preferential degradation of the PSII reaction centers relative to PSI. However, it is important to note that no significant genotypic effects in the composition of reaction centers and antenna proteins could be observed, and apparently there is no simple linkage between protein expression and the differential reduction in state transition observed for Antonia under Mn deficiency (Fig. 5, compare A with B–D).
Nonphotochemical quenching (NPQ) protects PSII from photoinhibition and was determined under light intensities equivalent to growth light (Table I
). When plants were exposed to Mn deficiency in growth light, NPQ was reduced by 53% in the Mn-inefficient genotype Antonia and by 38% in the Mn-efficient genotype Vanessa. In addition, a marked reduction in quantum yield of PSII (
The Chl a Fluorescence Induction Curve for Mn-Deficient Plants The leaf tissue concentration of Mn was clearly reduced below the critical threshold limit for Mn deficiency in barley plants in both the Mn-efficient genotype Vanessa and the Mn-inefficient genotype Antonia. Likewise, the induction of Mn deficiency resulted in a similar decrease in thylakoid Mn concentrations for both genotypes, but surprisingly, no difference in Mn concentrations was observed between the two genotypes (Fig. 2). However, the induction of Mn deficiency resulted in a number of marked changes to the Chl a fluorescence induction curves (Fig. 3). Especially, it should be noted that Mn deficiency resulted in marked differences between genotypes, at the same Mn tissue concentration, when the Chl a fluorescence induction curves were compared (Fig. 3). Thus, analysis of Chl a fluorescence induction curves as well as state transition results might constitute a powerful tool to diagnose Mn deficiency in plants well before it can be diagnosed visually.
In addition to the typical O-J-I-P steps on the fluorescence induction curves, the development of a clear K step at 0.2 to 0.4 ms was noticed in Antonia. The K step has previously been reported to be induced by heat stress (Srivastava et al., 1997
The second notable feature of the fluorescence induction curves from Mn-deficient Antonia was the appearance of a decline in the curve after the I step (Fig. 3), creating a so-called D step at 75 to 90 ms (Munday and Govindjee, 1969
The loss of adaptive mechanisms that optimize photosynthetic performance under varying light conditions or leading to diminished photoprotection may provide a mechanistic cause for a significant fraction of the grain yield reduction that occurs when barley plants are exposed to Mn deficiency. State transitions are considered to be one such adaptive mechanism. When PSII is favored over PSI, then excitation energy may be redistributed to PSI by changing the redox state of the thylakoids. A reduced pool of PQ is bound to the cytochrome b6f complex and activates a LHCII kinase, which phosphorylates Lhcb1 and Lhcb2 proteins and detaches a fraction of LHCII from PSII. Consequently, this LHCII migrates from PSII to PSI, leading to a preferential excitation of PSI and a rebalancing of light energy absorption between the two photosystems (Allen et al., 1981 The ability to perform state transitions was highly reduced in the Mn-inefficient genotype Antonia when exposed to Mn deficiency (Figs. 4 and 5A). The difference in state transitions between Mn-deficient genotypes is in good agreement with the observation that Mn-deficient plants and especially the Mn-inefficient genotype Antonia are less efficient at generating a reduced PQ pool, as approximated by the redox state of the PQ pool (1-qP; Table I), thereby initiating the redox-controlled phosphorylation of LHCII. However, the loss of state transitions in Antonia was apparently not due to a loss of light-harvesting complexes (Fig. 5B). Immunoblotting revealed no significant reductions in Lchb1 in the Mn-deficient samples and likewise no difference between the genotypes (Fig. 5B). However, detection of the phosphorylation levels of P-Lhcb1 and P-Lhcb2 showed a marked reduction in both genotypes under Mn deficiency (Fig. 5B), and clearly, no correlation between the amount of phosphorylated protein and the ability to perform state transitions could be observed. It appears that the observed difference in state transition might be influenced by (1) other proteins of the PSII reaction centers or antenna, (2) differential posttranslational modification of proteins expressed in equal amounts in the genotypes, or (3) specific changes in protein conformation.
NPQ declined by 40% to 50% in Mn-deficient plants, reflecting a situation where the donor side of PSII was under increased stress but the mechanisms of photoprotection had not been up-regulated (Table I). Marked reductions in
The increased vulnerability of the Mn-inefficient genotype Antonia to Mn limitation appears to be influenced by photochemical disturbances. When the two genotypes were supplied equally with low additions of Mn, the leaf tissue and thylakoid concentrations were similar. However, the Chl a fluorescence induction curves were markedly different between the genotypes, and the inefficient genotype Antonia had a reduced ability to perform state transitions, whereas the energy transduction in the efficient genotypes was much less affected. This observation might reflect a higher requirement for Mn in photosynthesis for Antonia, so that Mn becomes rate limiting at a higher physiological Mn concentration than in Vanessa. Alternatively, differences in the PsbA repair cycle, such as timely resupply of Mn to the photosystems, or differences in photoprotective mechanisms and susceptibility to damage from oxidative stress may also be important processes. These topics require further analysis. The results presented in this paper are consistent with Mn deficiency primarily targeting the OEC and affecting the donor side of PSII. Perturbations in the photosynthetic apparatus clearly involved a markedly reduced efficiency of PSII under Mn deficiency due to loss of the PSII core protein (PsbA). Thus, it can be concluded that even mild Mn deficiency without any distinct leaf symptoms may induce damages to PSII and consequently limit harvest yields, adaptability, and survivability of plants under field conditions.
Cultivation of Plants
Barley (Hordeum vulgare) was cultivated hydroponically in 4-L buckets, with four plants in each bucket. Seedlings were germinated on vermiculite, washed with distilled water, and then transferred to hydroponics. The composition of the nutrient solution has been described elsewhere (Husted et al., 2000 Barley genotypes with contrasting Mn efficiency (Mn-inefficient Antonia and Mn-efficient Vanessa) were precultivated for 1 week with ample supply of all essential nutrients. For the following 7 weeks, plants were split in two groups, either maintained at an ample nutrient supply (control) or transferred to a Mn-depleted nutrient solution. In order to induce Mn deficiency without development of leaf symptoms, 100 to 650 ng of Mn was added per plant per week, depending on the growth stage, whereas the control received 10 times this dosage. Additions of Mn to the nutrient solution and pH adjustment (pH 5.5–6.0) were made on a daily basis in order to limit the effects of a rapid and complete depletion of Mn when given as one weekly addition. This principle of daily additions ensured a more constant supply of Mn to the plants in both the low and control treatments.
Measurements of Chl a fluorescence were made using a hand-held portable fluorescence detector (Handy Plant Efficiency Analyser; Hansatech Instruments) to determine the maximum Fv/Fm. The leaves were dark-adapted for 30 min using leaf clips before measurement. Fluorescence measurements were recorded by illumination for 2 s with 3,000 µmol photons m–2 s–1 at a wavelength of 650 nm. The JIP test (Strasser et al., 2004
Thylakoid membrane isolations were made on approximately 1 g of leaf material from each bucket. Only the youngest, fully emerged leaves were used. Extractions were performed in the cold (5°C) under dimmed green light in order to maintain the integrity of the thylakoids. For homogenization, leaf material was transferred to a 50-mL Falcon tube with 30 mL of homogenizing buffer containing 0.4 M Suc, 10 mM NaCl, 5 mM MgCl2, 20 mM Tricine (pH 7.5), and 10 mM L-ascorbate. Samples were homogenized on an Ultra Turrax T25 (IKA) and then strained through Miracloth (pore size = 22–25 µm; Calbiochem). The extracts were centrifuged for 10 min at 5,000g, the supernatant was removed, and the pellet was resuspended in 5 mM Tricine (pH 7.9) and allowed to stand for 15 min in the dark in order to lyse the chloroplasts. Following lysis, the thylakoids were pelleted by centrifugation for 10 min at 12,000g, and the pellet was resuspended in a solution containing 0.4 M Suc, 10 mM NaCl, 5 mM MgCl2, 20 mM Tricine (pH 7.9), and 20% glycerol. NaF was added to all of the reagents at a final concentration of 10 mM as a phosphatase inhibitor. The samples were frozen immediately in liquid N2 and stored at –80°C until further analysis. The samples were stable for at least 3 months.
Leaf tissues of the youngest fully expanded leaf and thylakoid membranes were analyzed for elemental content with inductively coupled plasma-mass spectrometry (ICP-MS; model 7500ce; Agilent Technologies). Leaf samples were freeze dried using a Christ Alpha Freeze Drier (Martin Christ). Approximately 0.2 g of freeze-dried leaf was digested using 70 mL of polyethylene high-density vials (Capitol Vial) on a graphite heating block (Mod Block; CPI International). A modification of the Environmental Protection Agency method 3050 B was used, as described previously (Husted et al., 2004
NPQ, maximum
The fluorescence parameters (NPQ, 1-qP, and
State transitions were measured essentially as described by Lunde et al. (2000)
Total Chl was determined by methanol extraction of the youngest fully expanded leaf according to the method of Lichtenthaler and Wellburn (1983)
Thylakoid membranes were extracted 55 d after planting and used for immunoblotting. Twenty micrograms of total thylakoid proteins was separated by SDS-PAGE and transferred to a nitrocellulose membrane by blotting as reported previously (Jensen et al., 2000
Statistical analysis was undertaken using SAS (SAS Institute; version 8.2) for variance analysis and Student's t test for comparison of means. Mean values (X) are listed with the associated SE values (X ± SD/
The skillful assistance of Bente Broeng with ICP-MS and Lis Drayton Hansen with immunoblotting analysis are gratefully acknowledged. Received December 18, 2008; accepted April 4, 2009; published April 15, 2009.
1 This work was supported by the Ministry of Science, Technology, and Innovation (contract nos. 53–00–0234 and 274–06–0325), the Danish Grain Breeding Foundation, the Danish National Research Foundation, the Villum Kann Rasmussen Foundation, and the Danish Natural Science Research Council (contract no. 272–05–0360).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Søren Husted (shu{at}life.ku.dk).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.134601 * Corresponding author; e-mail shu{at}life.ku.dk.
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ABSTRACT
RESULTS
PSII) was also observed, describing a loss of photochemical efficiency in the Mn-deficient leaves. The PSII excitation pressure (1-qP) is an approximation of the relative fraction of reduced PSII (Rosenqvist and van Koten, 2003
PSII) were calculated using the following equations: 1-qP = (Fs – F0')/(Fm' – F0'), 
n).