Orinoquia

Orinoquia, Volumen 17, Número 1, p. 15-22, 2013. ISSN electrónico 2011-2629. ISSN impreso 0121-3709.

Documento sin título

ARTÍCULO ORIGINAL/ORIGINAL ARTICLE

Eficiencia fotoquímica del fotosistema II en plantas de brócoli (Brassica oleracea var Italica) afectadas por exceso de hierro

Photochemical efficiency of photosystem II (PSII) in broccoli plants (Brassica oleracea var Italica) affected by excess  iron

Eficiência fotoquímica do fotossistema II em plantas de brócolis (Brassicaoleracea  var Itálica) afetadas por excesso de ferro

Jaime E. Peña-Olmos1,  Fánor Casierra-Posada2

1     Agronomist, MSc, Plant Ecophysiology Research Group, Secretaría de Educación de Bogotá.

2     Agronomist, PhD, Plant Ecophysiology Research Group, Faculty of Agricultural Sciences, Universidad Pedagógica y Tecnológica de Colombia (UPTC). Tunja (Colombia) Email: jaime.pena@uptc.edu.co

Recibido: marzo 06 de 2012               Aceptado: mayo 16 de 2013

Resumen

Utilizando un diseño completamente aleatorizado, con tres tratamientos  y siete repeticiones  por tratamiento,  se determinó la fluorescencia  de la clorofila a en plantas de brócoli sometidas  a toxicidad por hierro. Como  material vegetal inicial se tomaron  plántulas de brócoli (Brassica oleracea var. Italica) híbrido Legacy de un mes de edad,  las que se sembraron  en contenedores de vidrio con una solución nutritiva, bajo invernadero  en Tunja – Colombia. Aproximadamente tres semanas después  del transplante  se adicionó  sulfato de hierro en concentraciones de 100 y 250 ppm de Fe, con un control sin aplicación de sulfato de hierro, para inducir reacciones  de las plantas al exceso del metal.  Diecisiete días después  de las aplicaciones  de Fe se realizaron las mediciones  de fluorescencia  de la clorofila, en hojas completamente expandidas y adaptadas a la oscuridad.  El análisis de varianza encontró diferencias significativas para todas  las variables evaluadas, excepto  para el coeficiente  de extinción no fotoquímica (qN). Los resultados indican que la toxicidad por exceso de hierro indujo un incremento en el nivel de estrés en las plantas de brócoli evaluadas, lo que afectó la eficiencia cuántica máxima y el rendimiento  fotoquímico operacional  del PSII (Fv/Fm  y )II, respectivamente), al igual que el coeficiente  de extinción foto- química de la fluorescencia (qP) y la tasa de transporte  de electrones.  Con lo anterior, es evidente  que el exceso de hierro modificó la fracción de energía de excitación destinada  para los procesos  fotoquímicos  y no fotoquímicos,  incidiendo  de forma directa en el proceso  fotosintético  de las plantas evaluadas.

Palabras clave: capacidad fotosintética, captura  de luz, centros  de reacción, exceso de energía, fotoinhibición.

Abstract

Acompletely  randomised  design,  having three  treatments  and  seven  repeats  per  treatment,  was used  for determining chlorophyll a fluorescence in broccoli  plants affected  by iron toxicity. One  month  old Legacy hybrid broccoli  seedlings (Brassica oleracea var. Italica) were taken as initial vegetal material and sown in a greenhouse in Tunja, Colombia, in glass vessels containing a nutritive solution. Iron sulphate at 100 and 250 ppm Fe concentration was added  about  three we after transplanting  (as well as control with out iron sulphate)  for inducing reactions  to the excess of metal in the plants. Chlorophyll fluorescence was measured in leaves which were fully expanded and adapted to the dark seventeen days after applying Fe. Analysis of variance (ANOVA) revealed significant differences for all the variables evaluated in this study, except for the coefficient of non-photochemical quenching  (qN).The results showed  that toxicity caused  by an excess of iron induced an increased  level of stress in the broccoli plants evaluated  here, there by affecting photosystem II’s (PSII) maximum quantumyield  (Fv/Fm), PS II operating  efficiency ()II), coefficient of photochemical quenching  (qP) and electron  transport rate. The foregoing makes it evident that an excess of iron modified the fraction of excitation energy destined  for photo- chemical and non-photochemical processes,  thereby having a direct impact on photosynthesis  in the plants evaluated here.

Key words: photosystem II (PSII),  photosynthetic capacity,  light capture,  photosynthetic reaction  centre,  excess energy, photo-inhibition.

Resumo

Usando um delineamento experimental inteiramente  casualizado,  com três tratamentos e sete repetições por tratamento, determinou-se  a fluorescência  da clorofila a em plantas  de brócolis submetidas  à toxicidade  de ferro. Como  o material inicial foram tomadas mudas de brocolis (Brassica oleracea var Itálica) Híbrido Legacy de um mês de idade, que foram plan- tadas em recipientes  de vidro com uma solução nutritiva em casa de vegetação em Tunja - Colômbia. Cerca de três semanas após o transplante  foi adicionado sulfato de ferro em concentrações de 100 e 250 ppm de Fe, com um controle  sem aplicação  de sulfato de ferro para induzir reações  das plantas ao metal em excesso. Dezessete dias após as aplicações  Fe foram realizadas medições  de fluorescência da clorofila em folhas completamente expandidas  e adaptadas a escuridão. A análise de variância foram encontradas diferenças significativas para todas as variáveis avaliadas, exceto para o coeficiente de extinção não-fotoquímica  (qN). Os resultados  indicam que a toxicidade  por excesso  de ferro induziu um aumento no nível de estresse  nas plantas de brócolis avaliados, afetando  a eficiência quântica  máxima e o desempenho fotoquímico operacional  do PSII (Fv / Fm e )II, respectivamente), do mesmo modo que o coeficiente  de extinção fotoquímica da fluo- rescência  (qP), e a taxa de transporte  de electrões.  Com o acima exposto, é evidente  que o excesso  de ferro modificou a fração energia de excitação destinada  a processos  fotoquímicos e não fotoquímicos participando  diretamente no processo de fotossíntese  nas plantas avaliadas.

Palavras-chave: capacidade fotossintética, captura  de luz, centros  de reação,  excesso de energia, foto inibição.

Introduction

Iron  is an  essential plant  nutrient; its functions  include  accepting and  donating electrons, and  it plays  an important role in the electron transport chain  for both photosynthesis and  respiration. Nevertheless, at  certain high levels of soil accumulation iron becomes to- xic to plants. Iron can act catalytically through Fenton’s reaction to  generate hydroxyl  radicals   that  damage fats, proteins, and DNA (Connolly and Guerinot, 2002). There is evidence that high iron concentrations can influence  growth  and  distribution of plant  species both in dry zones (Waldren et al., 1987)  and  humid  zones (Talbot et al., 1987).

Iron toxicity is often  seen  in irrigated  crops  as a result of excess  soluble  iron in irrigation water  (Ponnamperu- ma, 1976).  Iron toxicity is widely distributed in Asian, African, and South American  soils (Sahrawat, 2004).  In this sense,  the  phenomenon has been studied mainly in rice, due  to the  high levels of iron found  in poorly- drained acid  soils subjected to flooding  prior  to plan- ting  (De  Oliveira-Camargo, 1984).    Some  species of Asian rice (Oryza sativa) are  sensitive  to high levels of iron, especially  in its ferrous  form (Fe2+), and this sensi- tivity manifests  itself in symptoms such  as bronzing of older  leaves,  reduction in leaf growth  and  tillering, nutritional  imbalances, and  overproduction of ethylene (Majeruset al., 2007).

Colombia possesses  many  cultivable   soils,  of  which almost  all are  affected by some  problem such  as defi- ciency  or toxic excess  of certain  plant nutrients. In Colombia  there  are  areas  of lime soils with an excess  of mineral  salts, which  impede the  normal  development and growth  of cultivated plants.  Large areas  of the Caribbean plain,  the  Magdalena and  Cauca  floodplains, and  the  high altitude  plains, which  is to say the  major farming  zones of the  country,  are  susceptible to  salinization  (Casierra-Posada et  al., 2007).  On  the  other hand,  almost  67  million hectares in Colombia consist in acid  soils  affected by  iron  and  aluminum  toxicity (Casierra-Posada et al., 2008),  and  this is perhaps the major  limiting factor  for  crop  growth  in different  regions throughout the country (Malagón-Castro, 2011).

The savannahs of the Eastern Plains (also known  as the Colombian Orinoco region)  occupy some  17  million hectares (Molina et al., 2003),  of which 3.4 million hec- tares  of flat land that could  otherwise be used  for me- chanized agriculture possess Oxisols  and  other  soils with a pH of 4.5, low availability of Ca, Mg, K, and  P, and  high Al content (Flor, 2010;  Rodríguez-Atehortúa et al., 2010;  Cochrane y Sánchez, 1981).   These  soils are highly susceptible to degradation, and  under  natural conditions offer a poor  medium for production of crops  and pastures (Amézquita, 1998).

Despite the important plant  growth  limitations  caused by iron excess in Colombian soils (Gómez et al., 2007), there  has been little experimentation on  this topic.  In fact, much  global  research occurs in temperate zones with lime soils, where iron  deficiency and  not  excess is the  more  common problem (Prasad,  2003).  But the fact remains  that growth  and yields of the world’s prin- cipal crops  are drastically reduced by an excess  of this transition metal.  For example, rice cultivation  in a large  swathe of humid  lands  in Africa, Asia, and  South America   is strongly  affected by  the  generalized nutrient imbalance brought on by iron toxicity (Majeruset al., 2007).  Because of this, plant  physiological aspects should  be studied to understand the tolerance of diffe- rent  species to  iron  excess.  The objective of the  present  study  is thus to evaluate the  behavior of broccoli plants exposed to differing levels of iron in the growing medium.

Materials and methodology

The experiment was  carried  out  in a glass green house belonging to the Faculty of Agricultural and  Animal Sciences at  the  UPTC University  in Tunja,  Colombia. Average  temperature inside  the  greenhouse was 15.8 °C, relative  humidity  was 72.0%,  and photosynthetically-active radiation (PAR) was 650  µmolm-2s-1.

Planting  material  consisted in one-month-old broccoli plantlets (Brassica oleracea  var. Italica) of the  hybrid Legacy. These were  planted in glass containers containing a nutrient solution  with the following composition in mg  L-1:  nitrate  nitrogen 40.3;  ammonium nitrogen 4.0;  phosphorus 20.4;  potassium 50.6;  calcium  28.8; magnesium  11.4;   sulfur  1.0;  iron  1.12;   manganese 0.112;  copper 0.012;  zinc  0.0264; boron 0.106;  mo- lybdenum 0.0012; and  cobalt  0.00036. Twenty  days after transplanting iron sulfate  was added to the  plant to induce metal  excess,  in concentrations of 100  and 250  ppm,  with a control that  received no  iron sulfate excess.    Solution  pH  was  6.2  for the  control,  5.5  for the 100  ppm  iron treatment, and  5.3 for the 250  ppm treatment. The excess  iron  was  added gradually  over 20 days to avoid plant shock.

Chlorophyll   fluorescence was  measured 37  days  af- ter transplanting in dark-adapted leaves at ambient temperature using a Junior-PAM fluorometer (Walz GmbH,  Effeltrich, Germany). An actinic  pulse  of 820 µmolm-2s-1was  used.  Initial fluorescence (Fo), maximum fluorescence (Fm), effective   photochemical quantum yield of photosystem II or )II, quantum yield of light- induced non-photochemical quenching or Y(NPQ), quantum yield  of  non-light-induced non-photochemical quenching or Y(NO), electron transport rate  (ETR), a photochemical quenching coefficient (qP), an   nonphotochemical quenching coefficients (qN and  NPQ) were determined, and from thesevariable fluorescence (Fv) and maximum quantum efficiency of PSII (the ratio of Fv/Fm) were  calculated.

The greenhouse was fitted with pipes  and hoses  to ae- rate the glass containers, with the purpose of oxygena- ting plants. Experimental units were  laid out in a totally randomized design  with seven  replications of each  of the  three  treatments. Results were  subjected to analy- sis of variance (ANOVA), and  treatments were  compared  using  Tukey’s range  test  at a significance  level of 5%.  Statistical analyses  were  performed using version 19.0.0  of  the  IBM-SPSS statistics  program  (Statistical Product and Service Solutions,  IBM Corporation, New York, USA).

Figure 1. Minimum fluorescence (Fo) in plants of Brassica oleracea var. Italica exposed to iron toxicity (n=7).

Results and discussion

Minimum  fluorescence showed significant  differences between treatments (p<0.05),  progressively rising  as iron  content rose  in the  growing  medium. The value for this variable  was  26.0  and  40.6%  higher  in plants receiving  100  and  250  ppm  Fe, respectively, as com- pared to the control (figure 1).

Initial fluorescence values (Fo) can increase when  there is some  type of damage in the reaction centers of photosystem II (PSII) (Vieira et al., 2010),  or due to a reduction  in the  transfer  of excitation energy  from the  light harvesting complex to reaction centers (Baker and Ro- senqvist,  2004).  In the  same  way, the  loss of reaction centers as  a  result  of  damage in the  photosynthetic apparatus leads to an increase in the amount of energy emitted as Fo (Conroy  et al., 1986).   Photoinhibition of PSII related to stress  from iron excess  is accompanied by the oxidative  degradation of the D1 protein by light (Sárvári, 2005;  Suh et al., 2002),  and  iron excess  also causes deficiency of manganese, a crucial element for water   oxidation by  the  OEC  (oxygen   evolving  complex).

High iron concentrations in the growing  medium reduce the concentration of ions such  as Ca, Mg, and  P in apical  growing  points  and  thus  in plant  leaves,  which in turn  affects  the  photosynthetic apparatus of plants, given   that   these   nutrients  are   associated  with  the synthesis  of proteins involved  in the electron transport chain  and  other  aspects of photosynthesis (Majeruset al., 2007).  It can thus be assumed that magnesium deficiency  due  to  excess  iron  leads  to  the  synthesis  of fewer  primary  reaction  centers, and  this  raises  initial fluorescence and decreases the ratio of Fv/Fm, because this parameter is highly sensitive  to variations  in Fo and Fm.

Maximum  quantum efficiency  of PSII (Fv/Fm) showed significant   differences  for  the   different   treatments; this variable  diminished as iron concentration was raised.   Thus the  ratio  of Fv/Fm  was  respectively 5.4  and 11.1%  lower  in plants  under  100  ppm  and  250  ppm Fe treatments as compared to control plants (figure 2).

Xing et al., (2010)  found  that  maximum quantum efficiency  of PSII in Spirodela  polyrrhiza  was  reduced as iron  concentrations were   raised  in the  growing  solution, reaching a level of 0 with an iron concentration of 100  ppm.  By the  same  token,  Suh et al. (2000)  found that in pea plants exposed to iron toxicity, the values of Fv/Fm fell as compared to plants grown  under  optimum iron conditions. In both  studies,  the authors confirmed that  this  response of  maximum  quantum  efficiency of PSII is due  to  the  fact  that  high  concentrations  of the  metal  in plant  tissues  led to severe damage in the photosynthetic apparatus due  to reactive oxygen  species (ROS) (Xing et al., 2010),  which changed fatty acid composition in thylakoid  membranes and  thus altered their integrity (De Vos et al.,1991).  This would  interfere with the  biosynthesis of photosynthetic machinery, which   of  course  would   lower   photosynthetic rate (Yruela, 2005).

Figure 2. Maximum photochemical  quantum  yield of PSII (Fv/Fm) in plants of Brassica oleracea var. Italica exposed to iron toxicity (n=7).

Nenova (2006)  found  that  34  days  after  iron application  in garden pea,  maximum quantum efficiency  of PSII (Fv/Fm) showed no  significant  difference between treatments, though it did rise slightly until Fe concentration of 2 ppm,  and  began to  decrease as  iron concentration rose  from  10  to  40  ppm.  This author indicates that  reductions in  PSII maximum quantum yield are closely related to damage in the photo synthetic apparatus due  to  photoinhibition. In this same  experiment, there  were  no  significant  differences found between treatments for  other  aspects of  chlorophyll fluorescence, except for the  efficiency  in the  capture of excitation energy.  This implies  that  the  iron  levels used  in the  experiment were  not  sufficiently  high  or the  exposure sufficiently prolonged so as to induce a strong  inhibition  in activity of photosystem II.

One of  the  present study’s  most  important  findings relates  to electron transport rate.  As seen  in figure 3, significant  differences (p<0.05)  were  found  between the three  treatments evaluated. Plant exposure to iron toxicity  induced a  lower  ETR in broccoli plants,  with rates  40.5 and 67.6%  lower in plants subjected to 100  and 250  ppm  Fe, respectively, as compared to control plants.

Among  the  important symptoms related to  iron  toxicity  are  stunting  (De  Dorlodot et  al., 2005),  nutritio- nal disorders (Genon et al., 1994),  and  perhaps most importantly, the  overproduction of ethylene (Yamau- chi and  Peng,  1995).  This last reaction is possibly  the cause of a reduction in electron transport rate,  since ethylene  overproduction  reduces  the   useful   life  of plant  leaves,  and  thus  their  photosynthetic capacity. On the other  hand, Prasad  and Strzalka (1999)  suggest that  iron  and  copper excess  induces oxidative  stress in chloroplasts. When  reactive oxygen  species (ROS) reach  levels that  exceed a plant’s ability to extinguish them,  a peroxidation takes  place  in chloroplast membranes, which leads to a reduction in pigment concentration  (Baszynski et al., 1988),  causing  a low efficiency in photon capture and there  for in photosynthetic rate.

The   photochemical  fluorescence  quenching  coefficient   (qP)  and   the  non-photochemical fluorescence quenching coefficient related to heat dissipation (NPQ) presented significant  differences between treatments. Nevertheless, the  coefficient qN,  which  includes   all non-photochemical losses other  than  heat,  showed no significant   differences between  treatments,  possibly because, in the  toxic  conditions plants  were  exposed to, the most energetically economic way to release excess energy  was heat. Plants growing  with 100 ppm  Fe in the  substrate showed qP values  38.5%  lower  than controls, while  plants  in 250  ppm  Fe reduced qP  by 69.8%  as compared to control plants. NPQ was 36.8% lower in plants growing  under  100 ppm Fe than in con- trols, and 67.3%  higher in the 250 ppm  treatment than in the control treatment (table 1).

Figure 3. Electron transportrate (E TR) in Brassica oleracea var. Italica subjected to iron toxicity (n=7).

Table 1. Photochemical and non-photochemical quenching coefficients in plants of Brassica oleracea var. Italica exposedtoirontoxicity.

 

 

Iron (ppm)

 

Photochemical

Quenching

 

Non-Photochemical

Quenching*

 

Non-Photochemical

Quenching**

(qP)

(qN)

(NPQ)

 

Control

 

0.54 ± 0.14c

 

0.52 ± 0.03a

 

0.65 ± 0.26a

 

100

 

0.33 ± 0.08b

 

0.47 ± 0.15a

 

0.41 ± 0.09a

 

250

 

0.16 ± 0.05a

 

0.63 ± 0.15a

 

1.09 ± 0.47b


*   Coefficient of non-photochemical fluorescence quenching

** Non-photochemical fluorescence quenching: quantification  of non-photochemical quenching alternative to qN calculations. The extent of NPQ has been suggested to be associated with the number of quenching centers in the light-harvesting antenna. In each column, different letters indicate significant differences by variance analysis (p<0.05).#(n=7).

Regarding  the photochemical quenching coefficient (qP), Nenova (2006)  reported that  3 4  days  after  iron addition to pea  plants,  qP was  at its maximum under a concentration of 40 ppm  Fe. Nevertheless, the same author found  that  41 days after application, qP remained  at its highest  level for 0.1 ppm  Fe, but  that  upon raising concentration to 40 ppm,  qP decreased 2.3%. Despite the fact that differences were  not found  to be significant, it is important to note  that variations  in this parameter are  very sensitive,  such  that  a small change  can  indicate a  notable  modification in excitation energy  destined for primary  photochemical reactions in plants. In the same  respect, this author affirmed that NPQ (measured 41 days after iron application) rose  as iron concentration was raised from 0 to 40 ppm  in the growing  medium. This indicates a possible  instance of photoinhibition, since maximum quantum efficiency of PSII also decreased. The above implies  a higher  dissipation  of energy  in plants  grown  under  iron excess  as a  result  of  damage to  the  photosynthetic apparatus, which led to a reduction in qP.

Effective photochemical quantum yield of PSII, or )II, decreased as iron  concentration increased. Thus 100 and  250  ppm  applications of  Fe  reduced this  variable  by  38.0  and  66.4%  respectively as  compared to control plants. Non-photochemical fluorescence quen- ching  caused by factors  other  than  reductions in light harvest  (Y(NO)) also  presented significant  differences. Iron concentrations in the growing  medium of 100 and 250  ppm  raised  this variable  by 44.1  and  41.6%  respectively  in comparison to control plants.   For its part, non-photochemical fluorescence quenching due  to  a reduction in the  light harvesting function,  or  Y(NPQ), showed no significant differences between treatments (figure 4).

Figure 4. Excitation energy partitioning in Brassica oleracea var. Italica exposed to iron toxicity (n=7).

Referring    to   excitation   energy    partition,    Nenova (2006)  found  in garden pea  that  iron  applications up to 2 ppm increase effective photochemical yield of PSII ()II), both  at 34  days  and  41  days  after  the  onset  of application. This was  attributed principally  to the  fact that  low  doses of added Fe induce protein synthesis and  contribute to  the  proper functioning of the  photosynthetic apparatus. Nevertheless, when  this mineral was increased to concentrations of 10 and  40 ppm  in the  growing  medium, these  parameters began to  de- crease, and  though there  were  no  significant  differences found,  this reduction is pertinent to the discussion, since protein synthesis  is hindered by iron toxicity.  By the  same  token,  iron  excess  causes manganese deficiency in plants, which obstructs the electron transport chain,  thus  lowering  effective  photochemical yield of PSII ()II), while photochemical losses  increase, indicating some  type  of stress  on  PSII. In the  present study, the  differences in Y(NO) may  be  related to  the  pho- toinhibition of photosystem II, since  this parameter is linked  to  non-photochemical losses  other   than  heat dissipation (measured in turn  by Y(NPQ)), which  also showed significant  differences. Non-photochemical fluorescence quenching caused by factors  other  than the  reduction in the  light capture function,  or Y(NO), are  linked  to the  loss of energy  all along  the  electron transport chain, as well as to the destruction of the D1 protein in PSII .

Acknowledgments

This study  was  carried   out  with  the  support of  the Research Directorate (DIN) of the  Technological and Pedagogical University  of Colombia (UPTC), through the UPTC Young Researchers Program.   It also received support from the  Plant Ecophysiology  research group of the  Agricultural Engineering  program of the  Faculty of Agricultural and Animal Sciences of the UPTC.

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