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Plant, Cell and Environment
(2005) 28, 760-771 760
© 2005 Blackwell Publishing Ltd
Blackwell Science, LtdOxford, UKPCEPlant, Cell and Environment0016-8025Blackwell Science Ltd 2005? 2005
28?760771
Original Article
Respiration in sun and shade species
K. Noguchi
et al.Correspondence: Ko Noguchi. Fax:
81 6 6850 5808; e-mail:
address: knoguchi@bio.sci.osaka-u.ac.jp Response of mitochondria to light intensity in the leaves of sun and shade speciesKO NOGUCHI
1,2,3 , NICOLAS L. TAYLOR 2 , A. HARVEY MILLAR 2 , HANS LAMBERS 3 & DAVID A. DAY 2 1Department of Biology, Graduate School of Science, Osaka University, 1-1 Machikaneyama-Cho, Toyonaka, Osaka, 560-
0043, Japan,
2 Biochemistry and Molecular Biology, School of Biomedical and Chemical Sciences and 3School of Plant Biology,
the University of Western Australia, AustraliaABSTRACT
The present authors have shown previously that both res- piration rates and in vivo activities of the alternative oxi- dase (AOX) of leaves ofAlocasia odora
, a shade species, are lower than those in sun species, thereby optimizing energy production under limited light conditions (Noguchi et alAustralian Journal of Plant Physiology
28, 27-35,
2001). In the present study, mitochondria isolated from
A. odora leaves were examined in order to investigate the biochemical basis for the differences in respiratory param- eters.Alocasia odora
and spinach plants were cultivated under both high and low light intensities, mitochondria were isolated from their leaves, and their respiratory prop- erties compared. Mitochondrial content of leaf extracts from the two species was estimated using fumarase activi- ties and antibody detection of porin (the voltage-dependent anion channel of the outer mitochondrial membrane). On a mitochondrial protein basis, spinach leaves showed higher capacities of the cytochrome pathway and cytochrome c oxidase (COX) thanA. odora
leaves. However, on a mito- chondrial protein basis,A. odora
showed higher capacities of AOX, which had a high affinity for ubiquinone when activated by pyruvate.Alocasia odora
also had larger amounts of mitochondrial protein per leaf dry weight, even under severely shaded conditions, than spinach. Lower growth light intensity led to lower activities of most path- ways and proteins tested in both species, especially glycine- dependent oxygen uptake. In the low light environment, most of the AOX protein inA. odora
leaves was in its inactive, oxidized dimer form, but was converted to its reduced active form when plants were grown under high light. This shift may prevent over-reduction of the respira- tory chain under photo-oxidative conditions.Key-words
Alocasia odora
Spinacia oleracea
; alternative oxidase (AOX); mitochondria; respiration; sun and shade.INTRODUCTION
Plant mitochondria have two ubiquinol-oxidizing pathways,the cytochrome pathway and the alternative pathway. Thelatter consists of one enzyme, the alternative oxidase
(AOX), and has the potential to catalyse apparently waste- ful respiration in higher plant mitochondria. Its role in plants has not been definitively identified, except for heat production in the spadix of Araceae species, but it is thought to prevent production of reactive oxygen species (ROS) in the respiratory chain, especially under environ- mental stress (Vanlerberghe & McIntosh 1997; Moore et al2002; Vanlerberghe & Ordog 2002; Millenaar & Lambers
2003). However, many previous studies have imposed
severe physiological stresses on plants or cell cultures to induce changes in AOX activity or expression and conse- quently the ecophysiological role of AOX remains ambig- uous.In vitro
regulation of AOX involves alteration of the redox state of the AOX protein, activation by a -keto acids (e.g. pyruvate), and the redox state of ubiquinone (Q) (Day & Wiskich 1995; Siedow & Umbach 2000). However, regu- lation of AOX activity in vivo remains unclear (Millenaar & Lambers 2003), because (1) AOX protein is more often than not in the reduced, activated form in crude extracts of plant tissues (e.g. Millenaar et al . 2001); (2) the total pyru- vate concentration in cells is high enough to fully activateAOX, but the
in vivo pyruvate concentration in mitochon- dria is unknown (Siedow & Umbach 2000); and (3) the in vivo redox state of ubiquinone is rather stable (Millar et al1998; Millenaar
et al . 2001). These studies have led to the notion that most of the AOX protein is fully activated in vivo . Further analyses are required to understand the in vivo regulation and the physiological significance of AOX. Shade species show slower rates of leaf photosynthesis and respiration than sun species, contributing to a positive carbon balance under very low light conditions, such as Noguchi, Sonoike & Terashima 1996; Noguchi & Terashima1997).
In vivo
AOX activity in leaves of
Alocasia odora
, a shade species, is also low under light intensities similar to those in their natural habitat (Noguchi et al . 2001). Thus, inA. odora
leaves, the respiratory system appears to be geared towards efficient ATP production. In contrast, in leaves of spinach, a high-light adapted plant, in vivo AOX activity was high at the beginning of the night and then decreased during the night, when plants were grown under a high light intensity (Azcón-Bieto, Lambers & Day 1983;Noguchi
et al . 2001). Here we investigate the question of whether the leaves ofA. odora
have a smaller amount ofRespiration in sun and shade species
761© 2005 Blackwell Publishing Ltd,
Plant, Cell and Environment,
28,760-771
AOX or whether AOX is inactivated under low-light
conditions. Shade leaves within crops and other sun species, such as spinach, also show slower respiratory rates than leaves exposed to the sun (Noguchi et al . 1996).In vivo
AOX activity in leaves of spinach is also low under these condi- tions (Noguchi et al . 2001), ensuring high efficiency of res- piration, which may be advantageous in shaded environments in which photosynthetic production is low. Slower rates of photorespiration in shade leaves would also enhance net production of photosynthate (Muraoka et al2000). The photorespiratory pathway involves chloroplasts,
peroxisomes and mitochondria. In the mitochondria, gly- cine decarboxylase (GDC) converts glycine to serine, and produces NADH and NH 4 . We have also investigated the effect of light intensity on GDC and mitochondrial glycine oxidation.MATERIALS AND METHODS
Plant materials and growth conditions
We used
Spinacia oleracea
L., a sun species, and
Alocasia
odora (Lodd.) Spach., a shade species. Seeds ofS. oleracea
were purchased from a local supermarket in Perth, Austra- lia. The seeds were germinated in soil and 10 d later the seedlings were transferred to 20-L containers with hydro- ponic nutrient solutions. Plants ofA. odora
were propa- gated vegetatively from rhizome segments. The mother plant was purchased at a local nursery in Perth. Seedlings from the rhizome segments were transferred to 20-L con- tainers with hydroponic nutrient solutions. Twelve seedlings were grown in each container. For 1 week after transfer, the plants received one-eighth of the following solutions: 4 m M KNO 3 , 4 m M Ca(NO 3 2 , 1.5 m M MgSO 4 , 1.33 m M KH 2 PO 40.05 m
M ethylenediaminetetraacetic acid (EDTA)-Fe,0.01 m
M MnSO 4 , 1 m M ZnSO 4 , 1 m M CuSO 4 , 0.05 m M H 3 BO 3 , 0.5 m M Na 2 MoO 4 , 0.1 m MNaCl, 0.2
m M CoSO 4 Thereafter, the plants received the full nutrient solution. The pH of the nutrient solutions was adjusted to 6.0 using NaOH. The nutrient solutions were replaced once a week. The containers were placed in a walk-in growth chamber. In the growth chamber, day/night temperature and humid- ity were 25/20C and 60%, respectively, and the photope-
riod was 10 h. Black shade cloth was used to lower irradiance levels. The photosynthetic photon flux densities (PPFD) were 490, 200 and 20 m mol photons m 2 s 1 for high-light (HL), low-light (LL), and very low-light (VLL) conditions, respectively. As spinach did not grow under the VLL condition, we cultivated spinach under HL and LLquotesdbs_dbs48.pdfusesText_48[PDF] alpes de haute provence carte touristique
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