Chlorophyll fluorescence in rice: probing of senescence driven changes of PSII activity on rice varieties differing in grain yield capacity

Chlorophyll fluorescence in rice: probing of senescence driven changes of PSII activity on rice varieties differing in grain yield capacity

Antelmo R. Falqueto^I, Fabio S. P. Silva^II, Daniela Cassol^II, Ariano M. Magalhães Júnior^III Antônio C. Oliveira^IV and Marcos A. Bacarin^II*

^IUniversidade Federal do Espírito Santo, Departamento de Ciências da Saúde, Biológicas e Agrárias, Rodovia BR 101 Norte, Km 60, Bairro Litorâneo, CEP 29932-540 São Mateus, ES, Brazil. e-mail: [e-mail]

^IIUniversidade Federal de Pelotas (UFPel), Departamento de Botânica, Instituto de Biologia, CEP 96010-900 Pelotas, RS, Brazil. e-mail: [e-mail], [e-mail], [e-mail]

^IIIEmbrapa Clima Temperado, Caixa Postal 403, CEP 96001-970 Pelotas, RS, Brazil. E-mail: [e-mail] ⁽⁴⁾UFPel, Faculdade de Agronomia Eliseu Maciel, Departamento de Fitotecnia. e-mail: [e-mail]

Abstract

With Japonica rice BRS Firmeza and indica rice BRS Pelota (low and high grain yield, respectively) as materials, Chl content and Chl a fluorescence parameters in flag leaves from the heading to mature grain stage were investigated. The Chl content and the Chl a fluorescence were measured using a portable chlorophyll meter CL-01 and portables fluorometer Handy-PEA and FMS-2 (Hansatech, Kings Lynn, UK), respectively. All measurements were taken on middle part of the flag leaves (n = 10). The results showed that the Chl content and Chl a fluorescence parameters declined after full expansion of flag leaves in both rice cultivars. However, these biochemical and photochemical parameters did not show similar changing pattern and the behavior of flag leaves senescence showed some differences between BRS Pelota and BRS Firmeza rice cultivars. During the senescence of flag leaves, BRS Pelota, the rice cultivar with higher grain yield capacity, was characterized by significant reductions in Chl content, PI_ABS,Total, TR₀/ABS, ET₀/ABS, ET₀/TR₀, RC/ABS compared to BRS Firmeza. On the other hand, DI₀/RC, TR₀/RC and ET₀/RC were significantly higher in BRS Pelota. These results show that the decreased photosystem II activity, evaluated through chlorophyll fluorescence analysis, was resultant of leaves senescence process, which was much more expressive in BRS Pelota rice variety. We suggest that the higher productivity of BRS Pelota rice cultivar results from its higher assimilate mobilization ability or energy usage efficiency, in despite of its lower light absorption capacity.

Key words: JIP-test, non-photochemical quenching coefficient, Oryza sativa, performance index, PSII photochemical efficiency, stay green mutant rice.

Abbreviations: ABS/RC, absorption flux per RC; Chl, chlorophyll; DAH – days after heading; DI₀/RC, dissipated energy flux per RC; ET, conversion of excitation energy to electron transport; ET₀/RC, Electron transport flux per RC; ET₀/ABS = φ_Eo, quantum yield of electron transport; F₀, F_V, and F_M – minimal, variable and maximum Chl fluorescence of PSII in the dark adapted state; F_V/F_M = φ_Po= TR₀/ABS, maximal efficiency of PSII photochemistry; F₀’, F_V’ and F_M’ – minimal, variable and maximum Chl fluorescence in the light adapted state; F_V’/F_M’, efficiency of excitation capture by open PSII reaction centers; LD - constitutive non-photochemical loss in the dark; LNP - non-photochemical loss in PSII; ; NPQ Stern–Volmer quenching; qP, photochemical quenching; qN, non-photochemical quenching, φ_PSII, actual PSII efficiency; PI_ABS,Total, total performance index, measuring the performance up to the PSI end electron acceptors; PSI, photosystem I; PSII, photosystem II; Q_A, electron acceptor of PSII; qP, photochemical quenching coefficient; RC/ABS, ratio of reaction centers and the absorbance; RE₀/TR₀ = δ_R0, efficiency with which an electron can move from the reduced intersystem electron acceptors to the PSI end electron acceptors; TR, trapping of excitation energy; TR₀/RC, trapped energy flux per RC; φ_PSII, actual PSII efficiency; _Do quantum yield of dissipation; φ_Ro, quantum yield for the reduction of end acceptors of PSI per photon absorbed; RE₀/TR₀ = ρ₀, efficiency which a trapped exciton can move an electron into the electron transport chain from Q_à to the end electron acceptors of PSI; Ψ₀= ET₀/TR₀, yield of electron transport per trapped exciton.

INTRODUCTION

Leaf senescence is the sequence of biochemical and physiological events comprising the final stage of development (Jiao et al., 2003; Tang et al., 2005). The most striking event in leaf senescence is the disassembly of the photosynthetic apparatus with subsequent decrease in photosynthetic capacity (Lu et al., 2002; Weng et al., 2005). Previous studies have been shown that decreased photosynthetic capacity in senescent leaves may be associated with reduced photochemical activities of photosystems (Lu et al., 2002). Many studies relating the biochemical changes that occur during leaf senescence has focused on loss of photosynthetic pigments, degradation of protein, and re-absorption of mineral nutrients. Therefore, the drastic decline in activities of PSII, PSI and whole chain electron transport has also been reported in several senescing systems, indicating that the photochemical activity inhibits photosynthesis during leaf senescence (Zhang et al., 2006).

Among the experimental techniques available for investigation of photosynthetic activity in plants, Chl a fluorescence can be an excellent tool, giving us informations on the relationship between structure (molecular composition and conformation) and function of PSII. The use of this method to assess PSII photochemistry during leaf senescence in cultivars with differences in grain yield potential is important because it gives new insights about the fundamental processes of energy absorption and excess excitation energy use and dissipation by PSII in cereal crop plants during senescence. Moreover, such as already related in previous study, the leaf senescence pattern is variable and differences in leaf senescence should exist among cultivars with differences in grain yield (Falqueto et al., 2009a). In the present study, the fluorescence analysis according to so-called JIP-test will be used to compare the polyphasic rise of Chl a fluorescence between two rice cultivars differing in grain yield. This technical has been developed to investigate the “vitality” of plants in vivo and how it response to different environmental conditions (Srivastava and Strasser, 1996; Tsimilli-Michael and Strasser, 2008).

Efforts have been devoted to identify differences in chlorophyll fluorescence yield among rice varieties with differences in yield potential (Jiang et al., 2002). However, as far as Chl fluorescence parameters are concerned, the authors focused mainly on F_v/F_m and/or effective quantum yield of PSII (φ_PSII) (Lu et al., 2002; Jiang et al., 2002; Rapacz, 2007). Besides, the existing studies on the changes in Chl fluorescence parameters in rice with senescence were conducted on primary leaves or cotyledons (Yordanov et al., 2008; Mishev et al., 2009). Studies conducted on flag leaves of rice are still not available. Thus, the results obtained should give detailed information on the fundamental processes of energy absorption, utilization and dissipation of excess excitation energy by PSII during senescence of flag leaves in distinct rice varieties.

The aim of this study was to compare the physiological changes that occur on flag leaves of rice varieties during senescence. For this purpose, we made measurements of transient and modulated chlorophyll fluorescence and chlorophyll index of two rice varieties differing in grain yield potential (O. sativa subsp. indica BRS Pelota cultivar – high grain production and O. sativa subsp. Japonica BRS Firmeza cultivar – low grain production).

MATERIAL AND METHODS

Plant material: This experiment was carried during rice (Oryza sativa L.) growing season (October to March) during the summer 2007/2008 at the greenhouse of Institute of Botany, Federal University of Pelotas, Brazil (31º48’S, 52º24’W). The rice varieties used were BRS Firmeza (O. sativa subsp. Japonica) and BRS Pelota (O. sativa subsp. Indica). These cultivars were chosen because of their difference in grain yield potential (7.5 and 10 t ha^-1 for BRS Firmeza and BRS Pelota, respectively). BRS Firmeza is a stay green mutant rice included in the modern/american rice. BRS Pelota is originated through the selection of off-type plants found in a heterogeneous population of BR-Irga 410 cultivar. A randomized complete design with ten replicates was used for each rice cultivar. Each replicate consisted of one plastic pot (12 L) filled with soil fertilized according to official guidelines. Twenty-five seeds were sown in each pot. In order to obtain uniform plants, the seedlings of each pot were thinned from 25 to 5 per pot after the appearance of the second leaf. Thereafter, a water depth of 3 to 5 cm was maintained until after maturity. Flag leaves were sampled from the point of emergence of the head from its sheath (arbitrarily designated day 1) through senescence. All measurements were taken on middle part of the flag leaves. Ten replications of each parameter for each age were performed.

Chl content: The Chl content was estimated by portable chlorophyll meter (CL-01, Hansatech, Kings Lynn, UK). The results were express such as “chlorophyll index” (Cassol et al., 2008).

Chl transient fluorescence – JIP test: Polyphasic Chl a fluorescence transient (OJIP) was measured by means of Handy-PEA (Hansatech, Kings Lynn, UK). Before all measurements, leaves were dark-adapted for 20 min. Light intensity was 3000 μmol m^-2 s^-1, provided by an array of three high-intensity light-emitting diodes. The JIP-test (Strasser et al., 2004) was used to analyze each Chl a fluorescence transient. The concept of the JIP-test is based on the Energy Flux Theory in Bio-membranes (Strasser, 1981). These parameters provide structural and functional informations (such as specific and phenomenological fluxes, quantum yield or “vitality” indexes). The use of minimal (F_o) and maximal (F_m) fluorescence leads to the well accepted expression for the maximum quantum yield of primary photochemistry as TR₀/ABS = 1− (F_o/F_m) = F_v/F_m. For the detailed review on JIP-test parameters see Tsimilli-Michael and Strasser (2008). The performance index (PI_ABS,Total) (Tsimilli-Michael and Strasser, 2008) was introduced as a parameter to quantify the effects of environmental factors on photosynthesis in several studies.

Modulated Chl a fluorescence parameters: Modulated Chl a fluorescence was measured at room temperature with a portable fluorometer FMS-2 (Hansatech, Kings Lynn, UK) according experimental protocol described by Genty et al. (1989) and Roháček (2002). We measured minimal fluorescence (F_o) and maximal fluorescence (F_m) levels. Then, the leaves were continuously illuminated with a white actinic light (200 µmol m^-2 s^-1). The steady-state of fluorescence (F_s) was thereafter recorded and a second saturating pulse at 3000 µmol m^-2 s^-1 was imposed to determine the maximal fluorescence level in light-adapted leaves (F_m’). Then, the actinic light was removed and the minimal fluorescence level in the light-adapted state (F_o’) was determined through of illuminating the leaf with 1 s of far-red light. Using both light and dark fluorescence parameters, we calculated: a) effective efficiency of PSII photochemistry, when PSII reaction centers were open (F_v^’/F_m^’), b) the actual PSII efficiency (φ_PSII), c) photochemical quenching coefficient (qP) (Genty et al., 1989), d) the non-photochemical quenching coefficient (qN) (Genty et al., 1989), e) the Stern–Volmer quenching (NPQ) (Bilger and Bjorkman, 1990; Demmig-Adams, 1990), f) non-photochemical loss in PSII in dark-adapted state [LD = F_o/F_m] as introduced by Rohacek (2002), and g) non-photochemical loss in PSII [L_NP = F_o/F_m’], (Stefanov and Terashima, 2008).

RESULTS AND DISCUSSION

Senescence of flag leaves in two rice varieties differing in grain yield capacity was characterized by Chl loss (leaf yellowing), as well as decreases in activities of photosynthetic electron transport, evaluated thought Chl a fluorescence measurements. However, these photochemical and biochemical parameters did not show similar changing pattern and the behavior of flag leaves senescence showed some differences between BRS Pelota and BRS Firmeza rice cultivars. Chl index differed between rice cultivars during natural senescence (Figure 1A). Leaf Chl content of BRS Firmeza was significantly greater from 8 until around the 36 days after heading (DAH), after which they maintained without greatest variations with senescence. Chl index values increased gradually in BRS Firmeza until 14 DAH.

Since several decades, the degree of Chl loss has been strongly associated with light-saturated photosynthetic reaction during heading in rice (Jião et al., 2003). In the present study, the higher Chl content in BRS Firmeza during the flag leaf senescence shows that the process of leaf senescence in BRS Firmeza was delayed compared with the earlier senescent rice variety BRS Pelota. Thus, our results indicate that leaf senescence in BRS Firmeza was prolonged under natural conditions. BRS Firmeza is a stay green mutant rice, characterized by the persistence of the green color of leaves for longer than BRS Pelota rice variety.

It was observed a significant increase in ABS/RC in both rice cultivars after 25 DAH (Figure 1B). No difference in ABS/RC was observed between the cultivars. The performance index (PI_ABS,Total), which illustrate the vitality of photosynthetic apparatus (Tsimilli-Michael and Strasser, 2008), differed between the cultivars analyzed. In BRS Pelota rice cultivar, no significant variation of PI_ABS,Total was observed until 39 DAH. However, after this date PI_ABS,Total decreased significantly. In contrast, BRS Firmeza was characterized by an markedly increase in PI_ABS,Total after 1 DAH, which was maintained without greater variations until 25 DAH (Figure 1C). Reduced PI_ABS,Total values were obtained in BRS Firmeza after 25 DAH (Figure 1C).

Modulated Chl a fluorescence measurements were also performed on dark-adapted attached flag leaves of BRS Firmeza (low grain yield) and BRS Pelota (high grain yield) rice cultivars. Measurements were made on the 1^st, 18^th, 35^th and 46^th days after heading, corresponding to developmental stages R4 – Heading, R5 - Milk stage, R6 - Dough stage and R7 - Mature grain (Counce et al., 2000).

The Figure 2A shows biophysical parameters relative to PSII behaviour pattern: PI_ABS,Total, the efficiencies/fluxes ratios TR₀/ABS, ET₀/ABS, ET₀/TR₀ and RE₀/TR₀, the specific fluxes for trapping TR₀/RC and electron transport ET₀/RC, and the amount of photosynthetic reaction centres per absorption RC/ABS. In Figure 2 each chlorophyll fluorescence parameter was normalised according the control values (the data related to 1^st day were used as control). The energy fluxes are: for absorption (ABS); trapping (TR₀), i.e. reduction of Pheo (pheophytin) and Q_A; electron transport (ET₀) from Q_A^- to the intersystem electron acceptors - EA: Q_{B ­}(secondary electron quinone acceptor, PQ (plastoquinone), Cyt (cytochrome b₆/f) and PC (plastocyanin); reduction (RE₀) of end acceptors at the PSI electron acceptor side: NADP (nicotinamide adenine dinucleotide phosphate) and Fd (ferredoxin) (Tsimilli-Michael and Strasser, 2008).

The maximum quantum yield of primary photochemistry (TR₀/ABS), often the only fluorescence parameter used to gauge the occurrence and extent of physiological changes in plants, can be quite insensitive to change (Tsimilli-Michael and Strasser, 2008). In contrast, in the present study, the slight decrease in TR₀/ABS values was observed in both rice varieties at 46 DAH, as seen in Figure 2. However, in BRS Pelota, the rice cultivar disproved of stay green genes, TR₀/ABS values were much more reduced. In Addition, TR₀/RC showed a significantly increase at 48 DAH. This increase was more evident in BRS Pelota than in BRS Firmeza. The behavior pattern of TR₀/RC was also reflected in the increased values of effective antenna size per RC (ABS/RC – see Figure 1B). In BRS Pelota, the slower increase in ET₀/RC at 48 DAH resulted from an increase in trapping (TR₀/RC) and not from a reduction in the electron transport capacity (ET₀/TR₀).

In BRS Pelota the efficiency with which a trapped exciton can move an electron into the electron transport chain from Q_A^- to the intersystem electron acceptors (ET₀/TR₀) and the quantum yield of electron transport from Q_A^- to the intersystem electron acceptors (ET₀/ABS) were reduced in BRS Pelota at 46 DAH. In BRS Firmeza this parameters remained unchanged, except at 18 DAH (Figure 2B). The efficiency which an electron can be moved from the reduced intersystem electron acceptors to the end electron acceptors of PSI (RE₀/ET₀), the quantum yield of electron transport from Q_A^- to the end electron acceptors of PSI (RE₀/ABS), the efficiency which a trapped exciton can move an electron into the electron transport chain from Q_A^- to the end electron acceptors of PSI (RE₀/TR₀) decreased with senescence in both rice cultivars (Figure 2). However, the main difference between the rice cultivar was related to RC/ABS and PI_ABS,Total. In BRS Pelota these parameters were much more affected by senescence, while in BRS Firmeza there was an increased values of RC/ABS and PI_tot,ABS only at 18 DAH.

Thereafter, the specific fluxes (per RC), as well as the phenomenological fluxes (per cross section = CS) were not varied between rice cultivars except the heat dissipation capacity (DI₀/RC) (data not shown). DI₀/RC was higher in BRS Pelota at 46 DAH (developmental stage R₇), period that coincides with the decreased values of chlorophyll index and PI_ABS,Total. Also, high values of DI₀/RC have been associated to occurrence of photoinhibition. To date, photoinhibition has been conveniently measured as a lowering of the TR₀/ABS ratio following sufficient dark adaptation (Demmig and Björkman, 1987). DI₀/RC indicates the rate of the total dissipation of untrapped excitation energy from all RCs with respect to the number of active RCs. Dissipation in this context refers to the loss of absorbed energy through heat, fluorescence and energy transfer to other systems (Strasser et al., 2004) Therefore, dissipation can be also thought of as the absorption of photons in excess of what can be trapped by the RC. The DI₀/RC values can be influenced by the ratio of active/inactive RCs. Thus, analyzing the DI₀/RC values we can predict the proportion of RCs inactive in a sample.

From our results, we observed a greater variation of F_v’/F_m’ and φ_PSII values in both rice varieties with senescence. F_v’/F_m’ and φ_PSII decreased significantly from 8 DAH until 18 DAH, increasing again until 38 DAH at which point it decreased significantly until 48 DAH (Figure 3). Note that the variations in F_v’/F_m’ approximately paralleled the variations in effective quantum yield of photochemical energy conversion in PSII (φ_PSII) in BRS Pelota and BRS Firmeza. Therefore, this variation was similar between rice varieties, showing that the two rice varieties present the same efficiency of use the excitation energy during the light-adapted state. According to Stefanov and Terashima (2008), decreases in F_v’/F_m’ and φ_PSII could be associated with an increased non-photochemical loss. However, in this study, no clear relationship was observed between F_v’/F_m’ and φ_PSII values and those non-photochemical quenching (qNP) (data not show). In this development stage, decreases in F_v’/F_m’ and φ_PSIIwere followed by the slight increase (but not significant) in L_NP, corroborating the statement made by Lu et al. (2002) and Stefanov and Terashima (2008). qNP was higher in BRS Pelota until 6 DAH. However, it values were lowering in BRS Pelota from 36 DAH until 48 DAH (Figure 3C). qP, L_D and L_NP were unchanged in both rice varieties by senescence (data not shown).

The results of this study show that the fast Chl a fluorescence transient measurements with high time resolution provide a non-invasive and rapid method to study PSII activity changes caused by senescence. Since senescence induces structural disorganization, a general trend in the disorganization of the photosynthetic apparatus during senescence could be visualized in rice varieties differing in yield capacity. In addition, although this manuscript does not focused in explain the differences in grain yield of rice cultivars by means of chlorophyll fluorescence investigations, concerning the physiological significance of the senescence and its relationship with assimilate partitioning in plants, we suggest that the higher productivity of BRS Pelota rice cultivar results from its higher assimilate mobilization ability (Falqueto et al. 2009b), in despite of its lower light absorption capacity. These results are supported by that lowest Chl content and lower values of PI_ABS,Total, TR₀/ABS, ET₀/ABS, ET₀/TR₀, the amount of photosynthetic reaction centres per absorption (RC/ABS) and higher F₀, DI₀/RC, specific fluxes for trapping (TR₀/RC), electron transport (ET₀/RC) obtained in BRS Pelota during senescence (mainly at 46 DAH).

The results of this study showed that rice varieties differing in grain yield were characterized by significant differences in the capacity of absorption and use of light. BRS Pelota, the rice cultivar with higher grain yield capacity was characterized by lowest Chl content and lower values of PI_ABS,Total, TR₀/ABS, ET₀/ABS, ET₀/TR₀, the amount of photosynthetic reaction centres per absorption (RC/ABS) and higher F₀, DI₀/RC, specific fluxes for trapping (TR₀/RC), electron transport (ET₀/RC). These results show that the decreased photosystem II activity, evaluated through chlorophyll fluorescence analysis, was resultant of leaves senescence process, which was much more expressive in BRS Pelota rice variety. We suggest that the higher productivity of BRS Pelota rice cultivar could be more correlated with energy usage efficiency or assimilate mobilization rather than with their light absorption capacity.

Received: 01 February 2010; Accepted: 11 April 2010

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Publication Dates

• Publication in this collection
  23 July 2010
• Date of issue
  2010

History

• Received
  01 Feb 2010
• Accepted
  11 Apr 2010