REVIEW
Plant respiration under low oxygen 1*
Guillermo Toro , and Manuel Pinto
2
Respiration is an oxidative process controlled by three pathways: glycolysis, the tricarboxylic acid (TCA) cycle, and oxidative phosphorylation (OXPO!)" Respiratory #etabolis# is $bi%$ito$s in all organis#s, b$t with di&&erences a#ong each other" 'or exa#ple in plants, beca$se their high plasticity, respiration involves #etabolic pathways with $ni%$e characteristics. In this way, in order to avoid states of low energy availability, plants exhibit great flexibility to bypass conventional steps o& glycolysis, TCA cycle, and OXPO!" To $nderstand the energetic lin between these alternative pathways, it is i#portant to now the growth, #aintenance, and ion $ptae co#ponents o& the respiration in plants" Changes in these components have been reported when plants are subjected to stress, such as oxygen deficiency. This review analyzes the c$rrent nowledge on the #etabolic and &$nctional aspects o& plant respiration, its co#ponents and its response to environ#ental changes" ey words: lectron transport chain, hypoxia, *rebs cycle, #aintenance respiration"
I!TR"#$%TI"! Plants are a$totrophic organis#s able to $se solar radiation
its #echanis#s o& reg$lation and control still re%$ire &$rther el$cidation" 'or instance, st$dies on the enzymatic functionality of glycolysis have determined the
to split water #olec$les ( +O) and red$ce the carbon dioxide (CO +) compounds that can finally be stored as insol$ble polysaccharides (starch) or $sed directly in the synthesis o& other co#po$nds" n plants gl$cose is the #ain s$bstrate &or respiration" This process oxidizes carbohydrates through two principal pathways: glycolysis and the tricarboxylic acid (TCA) cycle" The prod$cts &ro# these two pathways are CO+ and the red$ced co#po$nds -A.(P)+ and 'A.+, which in t$rn are $sed &or oxidative phosphorylation (OXPO!), trans&erring their electrons to the ter#inal oxidase where O + acts as the final electron acceptor, producing high energy phosphate bonds (ATP) (/illar et al", +0112 van !ongen et al., "#$$). %T& represents the most efficient way to obtain energy &or the synthesis o& bio#olec$les and
i#portance o& phosphogl$co#$tase (P>/) in starch &or#ation processes in both heterotrophic (root and seed) and a$totrophic tiss$es as well as the role o& hexoinases *123) and other enzymes such as the glucose signaling networ (!heen, +015)" Regarding the TCA cycle, so#e progress has been #ade in $nderstanding how alternative pathways involving 4aminobutyric acid *5%6%) and the glyoxylate cycle operate, with special attention given to changes in the opti#al condit ions, in order to show the high level o& plasticity in the response o& the TCA cycle to environ#ental changes (!weetlove et al", +010)" /ore details will be given in another section below" 7n the other hand, research has been directed at finding new nonphosphorylates or alternative pathways &or
to #aintain cell$lar str$ct$res, transport photoassi#ilates, $ptae ions, assi#ilate - and !, reg$late protein t$rnover and #aintain electroche#ical potential gradients across #e#branes in cells (A#thor, +000)"
oxidase (AOX) is a protein associated with the inner #itochondrial #e#brane, it has been shown to be ind$ced by a series o& stress &act ors s$ch as high and low temperatures, drought, and nutrient deficiency , among others (/oore et al", +00+)" '$rther#ore, alternatives have also been &o$nd to the #aintenance o& the proton gradient in the #itochondrial #atrix, which is per&or#ed thro$g h uncoupled proteins *8'&) that enables flows of protons to enter the #atrix independent o& ATP synthesis (Arnholdt!ch#itt et al", +006)" n t$rn, ?CP wo$ld participate in the red$ction o& reactive oxygen species (RO!), a &$nction also contrib$ted to by AOX (!#ith et al", +005)"
Plant respiration has been widely st$died, b$t despite this e&&ort and the available new technologies, 1
'entro de (studios %vanzados en ruticultura *'(%), 'amino +as &arcelas ", sector +os 'hoapinos, -engo, 'hile. 3 Corresponding a$thor (g$iller#otoro4g#ail"co#)" +
Instituto de Investigaciones %gropecuarias, II% +a &latina, /anta -osa $$0$#, +a &intana, /antiago, 'hile. Received: 20 December 2014. Accepted:
7 May 2015. doi:10"50678!0719 ;9<=+01;000<00007
OXPO! that allow energy to be dissipated" Alternative
Respiration plays an i#portant role in accli#ation to di&&erent types o& abiotic stress (water, te#perat$re,
C@A-O?R-A@O'A>RC?@T?RA@R!ARC7;(!$ppl"1)A?>?!T+01;
;7
photoinhibition, salinity, nutrient deficiencies, and hypoxia8anoxia, etc"), there&ore #any st$dies have focused on understanding the function, organization, and reg$lation o& respiratory #etabolis# $nder $n&avorable environ#ents" These stresses $s$ally res$lt in changes in the energy re%$ire#ents o& plants, which in t$rn ind$ce changes in respiratory #etabolis# as well as in other enzymes, electron transport, and redox gradient &or#ation, a#ong others" One i#portant stress that affects respiration is partial deficiency *hypoxia) or absol$te absence (anoxia) o& oxygen" 'or
&ro# co#plete oxidation o& hydrocarbon s$bstrates, both in plants and ani#als (Plaxton, 1==6)"
instance, $nder hypoxic conditions alanine creates a lin to glycolysis (de !o$sa and !ode, +00<)" /oreover, $nder anoxia, &er#entative lactate and ethanol pathways are activated and the rate o& ethanol synthesis rises #ore than ; &old as co#pared to nor#al conditions (/anc$so and /arras, +006)" 6ecause of this concern, the objective of this review was to analyze the state of the art of plant respiration, both in ter#s o& #etabolis# and &ro# a &$nctional point of view. or this reason, in the first part of this review, a co#parative analysis o& the #aBor
Th$s, a st$dy in e$calypt$s plants showed that lea& respiration is highly dependent on both radiation and te#perat$re, showing a high degree o& inhibition o& respiration at high te#perat$res and high radiation levels, which red$ces the CO + ratio (provided by photosynthesis) that is respired (Atin et al", +000)"
#etabolic pathways o& aerobic respiration in ani#als and plants is per&or#ed"
what #ost a&&ects root respiration (>$pta et al", +00=)" This &actor is
Then, after analyzing recent advances in 9nowledge abo$t the &$nctionality o& respiration in plants beyond its traditional role as an energy generating process, we disc$ss in partic$lar its role in the synthesis o& new co#po$nds and in the #aintenance o& #olec$les and str$ct$res" Consideration is partic$larly given to &$nctions $nder di&&erent inds o& stress" 'inally, the response o& di&&erent parts o& the anaerobic respiration syste# to oxygen restrictions and the &$nctionality o& alternative #etabolic pathways activated in plants when oxygen is restricted (i"e" d$ring hypoxia) are disc$ssed"
electron acceptor in 72&17/
"&er&iew o' plant respiration Respiration involves the participation o& di&&erent processes responsible &or the oxidation o& gl$cose #olec$les &or energy and C str$ct$res, either in the presence (aerobic) (/illar et al", +0112 van .ongen et al", +011) or absence (anaerobic) o& oxygen (>$pta et al",
+00=)" n the latter case, the #ost a&&ected organ is the root, ind$cing partial oxidation strategies o& s$bstrates in order to contin$e to generate energy witho$t oxygen (O+)" These strategies are called &er#entation, which di&&erentiate the#selves by their end prod$cts: ethanol, lactic acid and alanine (!o$sa and !ode, +00+)" n the presence o& O +, s$bstrates are co#pletely oxidized to '7 + and +O (van .ongen et al", +011)" This is done thro$gh three #etabolic processes: glycolysis, the TCA cycle and the OXPO! ('ernie et al", +005)" To these is added a &o$rth process2 transport o& the prod$cts o& respiration" This corresponds to the #ove#ent o& s$bstrates and co&actors to &acilitate the release o& prod$cts thro$gho$t the cell (/illar et al", +011)" The operation o& these processes is the most efficient way to obtain energy ;9
t has been reported that there are di&&erences in respiration according to species and plant tiss$e (/illar et al", +011)2 &or exa#ple, spinach lea& respiration is pre&erably per&or#ed at night, beca$se d$ring the day it is inactivated + 1
at low solar radiation intensities (10;0 #ol # s ) (Atin et al", 1==9), pres$#ably ca$se excess ATP &ro# photosynthesis in chloroplasts (Atin et al", +005)" owever, &or #any years the e&&ects o& radiation on lea& respiration were st$died witho$t considering the e&&ect o& te#perat$re"
+i9ewise, root respiration can be altered by a variety of &actors s$ch as te#perat$re (Rach#ilevitch et al", +006), salinity
*6ernstein et al., "#$), heavy metals *;oyen and -oblin, "#$), drought *
however, the availability o& O + is ey in respiration #etabolis#, because oxygen is the final (/oller, +001)" /ost o& the energy (ATP) prod$ced by root respiration is $sed &or processe s s$ch as growth (van ersel
and
/eymour, "###> Thongo ;?6ou et al., "#$#), nitrate reduction, symbiotic fixation *in legumes), the absorption o& nitrate and other ions absorption by the roots (Poorter et al., $@@$), protein turnover *!e Aisser et al., $@@"> 6ouma et al", 1==52 !che$rwater et al", +000), #aintenance o& the ion gradient and #e#brane potential (Deen, 1=902
6ouma
and
!e
Aisser,
$@@)
and
waste
mechanisms and prod$ction o& heat thro$gh alternative pathways (Cannell and Thornley, +000)" Gly(olysis in plants >lycolysis is an anaerobic pathway responsible &or oxidizing sucrose *glucose in animals) to generate %T&, a red$ctant (-A.) and pyr$vate (/illar et al", +0112 van .ongen et al", +011)" The $niversality o& glycolysis is associated with its i#portance in adaptations to di&&erent environ#ental stressors, s$ch as n$tritional stress, te#perat$re, dro$ght, and anoxia, a#ong others (Plaxton, 1==6)" n general, the trans&or#ation o& gl$cose to pyr$vate is per&or#ed thro$gh a series o& reactions catalyzed by numerous enzymes *igure $) *&laxton, 1==62 van .ongen et al", +011), which not only act as catalysts and energy #etabolis# reg$lators (Ca#acho Pereira et al", +00=), b$t also as signal trans d$cers in response to changes in the environ#ent" 'or instance, it has been observed that the activity level o& hexoinase (X*) wo$ld correspond to a ey co#ponent in the s$gar signal detection" 'or exa#ple, it was deter#ined that X* (AtX*1) reg$lates the signaling levels o& s$gar
C@A- O?R-A@ O' A>RC?@T?RA@ R!ARC 7; (!$ppl" 1) A?>?!T +01;
!o$rce: A$thor based on Plaxton (1==6) and Plaxton and PodestE (+006)" (nzymes involved in each reaction are as follows: $) sucrose synthase, ") invertase, ) phosphorilase, B) C and Damylase, E) !& 9inase, 0) fructo9inase, i
7) hexoinase, 9) ?.Pgl$cose pyrophosphorylase, =) p hosphogl$co#$tase, 10) phosphogl$cose iso #erase, 11) ATPP'*, 1+) PP P'*, 1<) aldolase, 15) triose phosphate, 1;) and 16) glyceraldehyde<phosphate phosphorylated and nonphosphorylated, respectively, 17) phosphoglycerate inase, 19) F
F
phosphoglycero#$tase, 1=) enolase, +0) PP phosphatase, +1) ATPasa, ++) pir$vate inase, and +<) PPiasa" Figure 1. Schematic represent ation of the glycoly sis pathway and alternative s in veget ables . Continuous line represent s )roen lines represent alternati&es+ glycolytic flux and
in Arabidopsis gin2 #$tants $nder di&&erent lighting conditions" -or#al growth was observed in control plants2 however, in #$tant plants (gin2/h!1), growth was inhibited d$e to a red$ction in cell expansion (/oore et al", +00<)"
n t$rn, X* activity in plants is related to the lin between glycolysis and progra##ed cell death *apoptosis). 6riefly, mitochondrial pathways of apoptosis are initiated by #itochondrial cytochro#e c release (high control point o& apoptosis initiation) into the cytoplas#
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59
thro$gh pores in the #itochondrial per#eability transition (/PT) in response to so#e stress (*i# et al", +006)" X* is an integral co#ponent o& /PT, thro$gh its interaction with porins (D.AC, Doltage .ependent Anion Channel)" Ghen X* binds to D.AC it inter&eres with the opening o& /PT, inhibiting the release o& cytochro#e c into the cytoplas# and hence inhibiting apoptosis (*i# et al", +006)" been attrib$ted n ani#als, apoptotic activity has to the action o& n$clear glyceraldehyde<phosphate dehydrogenase (>AP.) on c$lt$red ne$rons" /oreover,
&$nctionally associated with #itochondria (>iegH et al", +00<)" /oreover, in bean ( "haseo#$s v$#garis +.) it was found that the enzymes phosphoglycerate 9inase * P>*), >AP., and aldose are associated with the n$clei and cytoseletons o& lea& cells, while in corn, <P>* and aldose are only associated with the cytoseleton *%zama et al., "##). The glycolytic flux is controlled
by a cascade o& reactions in which there are checpoints on the pathw ay, s$ch as X* and P* activity, which can control glycolysis not only at the #itochondrial level b$t also &ro# a posttranslational level"
it has been observed that X* #ediates the signaling o& sugars on the %6% pathway. Thegin1 #$tant is allelic to aba, which has been found to act on an enzyme that catalyses the last step in %6% biosynthesis, indicating that 123 level mediates signaling by the %6% pathway (Rolland et al", +00+)" n addition, protective &$nctions against RO! have also been attrib$ted to a #itochondrial X* thro$gh the generation o& A.P &or OXPO!, avoiding li#itations in the synthesis o& ATP d$ring respiration and &acilitating the release o& hydrogen peroxide (Ca#achoPereira et al", +00=)" Ghile X* is &o$nd in the #itochondria, there is also evidence to indicate the presence o& X* in the cell n$cle$s (*i# et al", +006)" This wo$ld indicate that X* #ight be controlled at the level o& glycolytic gene expression" %lthough each enzyme involved in the glycolytic flux corresponds to a critical control point in respiration, it was observed that altering the activitiesof these enzymes caused only minor changes inrespiration rates *1ajirezaei et al", +0062 Oliver et al", +009)" This indicates that there are other ey points in the reg$lation o& respiration" !t$dies in di&&erent organis#s (bacteria and #a##als) show that one o& the ey sites o& reg$lation and control o& respiration is at the level o& pyr$vate inase (P*), which catalyzes the final reaction in the pathway using %!& and phosphoenolpyr$vate (PP) &or ATP and pyr$vate *Teusin9 et al., "###). +i9ewise, in plants the situation is co#plex beca$se there are vario$s iso&or#s o& the sa#e enzymes, such as &3 *&laxton and &odestF, "##0). ?nlie other organis#s, glycolysis in plants can be carried o$t in two di&&erent s$bcell$lar co#part#ents, in
Tri(ar)oxyli( a(id (y(le in plants The tricarboxylic (TCA) cycle, also called the *rebs cycle in honor o& its discoverer, is an essential #etabolic pathway" t is located in the #ito chondrial #atrix where, by the oxidation o& organic C s$bstrates (pyr$vate and8or #alate), it releases CO + and provi des red$cing &actors s$ch as -A.(P) and 'A.+, which are pri#ary s$bstrates &or the synthesis o& ATP in the electron transport chain in #itochondria ('ernie et al", +0052 /aillo$x et al", +0072 !weetlove et al", +010) ('ig$re +)" n t$rn, the TCA cycle provides C seleton co#ponents and prec$rsors &or the biosynthesis o& secondary #etabolites s$ch as terpenes, a#ino acids, and &atty acids, a#ong others (Plaxton and PodestE, +0062 !weetlove et al", +010)" The TCA cycle begins with the reaction between acetyl CoA and oxaloacetate (OAA), yielding tricarboxylic acids that are oxidized and decarboxylated through a series of reactions in which CO+ #olec$les are released" At the end o& the cycle, OAA is regenerated &or recondensation with acetyl CoA, restarting the cycle ('ig$re +) (/aillo$x et al", +0072 !weetlove et al", +010)" One o& the #ain di&&erences between the TCA cycle in plants and ani#als is the energy #olec$le generated d$ring the processing o& s$ccinyl CoA to s$ccinate" Ghile ATP is prod$ced by s$ccinyl CoA synthase in plants, in animal cell there are two isoforms, 5T&specific succinyl 'o% synthase *5/'/) and %T&specific succinyl 'o% synthase, which generate g$anosine;Itriphosphate (>TP) &ro# g$anosine diphosphate (>.P) and ATP &ro# A.P, respectively (ohnson et al", 1==9)"
the cytoplas# and plastids (chloroplast and a#yloplast)" This ma9es it difficult to analyze and understand, because it involves interactions and connectivity thro$gh highly selective transporters, together with the interactions o& about " different enzymes *&laxton, $@@0> ;uGoz 6ertomeu et al., "#$#). have paid special attention n ani#al cells st$dies to the spatial organization of glycolysis, because the physical concentrations of glycolytic enzymes may be associated with sites with high demand for %T& *+u et al", +0012 >iegH et al", +00<) or other inter#ediates o& glycolysis (>iegH et al", +00<2 'ernie et al", +005)" A st$dy in Arabidopsis established that the enzymes X*, >A.P, and phospho&r$ctoinase (P'*) were
Another &eat$re associated with the TCA cycle in plants, b$t not &o$nd in other organis#s, is related to the significant activity of %!dependent malic enzyme
60
(-A./) or #alate oxidored$ctase, responsible &or catalyzing the oxidative decarboxylation of malate to pyruvate, finally allowing complete oxidation of malate
(enner et al", +001)" Patways asso(iated wit te T%- (y(le in plants There are several alternative pathways in the TCA cycle, which give some flexibility against environmental changes or si#ply in the choi ce o& which co#p o$nds to biosynthesize */weetlove et al., "#$#). or instance, 4 aminobutyric acid *5%6%) was long considered just a
C@A- O?R-A@ O' A>RC?@T?RA@ R!ARC 7; (!$ppl" 1) A?>?!T +01;
!o$rce: A$thor based on Ryan et al" (+001) and !t$dart>$i#araes et al" (+007)" &(&: &hosphoenolpyruvate, 7%%: oxaloacetate, //%: succinyl semialdehyde, //%!1: succinyl semialdehyde dehydrogenase, 5%6%: 4 aminobutyric acid, 5%6%T: 4aminobutyric acid transaminase, 5%!: glutamate decarboxylase, 5lu: glucose, %la: alanine, &ir: pyruvate.
(nzymes involved in each reaction are as follows: $) enolase, ") pyruvate 9inase, ) pyruvate dehydrogenase, B) coenzyme %, E) citrate synthase, 0) aconitase, 7) isocitrate dehydrogenase, 9) +oxogl$tarate dehydrogenase, =) s$ccinyl CoA synthase, 10) s$ccinate dehydrogenase, 11) &$#arase, 1+) #alate dehydrogenase, 1<) phosphoenolpyr$vate carboxylase, 1 5) isocitrate lyase, 1;) #alate synthase" .igure 2+ /(emati( representation o' tri(ar)oxyli( a(id (y(le 0T%- in plants+ Red line T%- (y(le, green line glyoxylate (y(le, gray line G-3- route+
#etabolite in plants with an $nclear &$nction2 however, at present there is evidence to indicate that 5%6% plays a #aBor role in C #etabolis# in response to stress
stress responses (*innersley and T$rano, +000)" ?nlie in plants, in mammals 5%6% clearly functions as a molecular neurotransmitter in the brain *6ouch= and
*6ouch= and romm, "##B). %s shown in igure ", the 5%6% pathway is composed of three enzymes> glutamate decarboxylase *5%!), a cytoplasmic enzyme, and two mitochondrial enzymes called 5%6% transaminase and succinicsemialdehyde dehydrogenase *5%6%T and
'ro##, +005)" The glyoxylate cycle is another pathway associated with the T'% cycle in plants, defined as a modification o& the TCA cycle ('ig$re +) (*ornberg and /adsen, 1=;9)" n t$rn, it has #ainly been associated with lipid #etabolis# in seeds o& oil plants (ast#ond and >raha#, +001)" n general, the di&&erence between glyoxylate cycle and T'% cycle is that the first avoids two points o& decarboxylation and allows the generation of acetyl 'o% through D oxidation of fatty acids, giving rise to s$ccinate, which is then incorporated into the #itochondria to generate OAA, which will go directly toward the synthesis o& s$crose by gl$coneogenesis (ast#ond and >raha#, +001)"
!!A., respectively), present both in ani#als and plants *6ouch= and romm, "##B> /weetlove et al., "#$#). In plants, it has been observed that 5%6% pathway responds %$icly to environ#ental changes, e"g" it is sti#$lated $nder conditio ns o& cold, salinity (*innersley and T$rano, +000), and anoxia (A$risano et al", 1==;)" The role of 5%6% pathway in plants is still unclear because st$dies on this pathway are relatively new" owever, it could be that 5%6% pathway is lin9ed to many abiotic
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61
n oil seeds, the #ost i#portant so$rce o& storage s$pply is lipids, which are $sed by the glyoxylate cycle to #aintain growth and respiration o& the seed" 'or exa#ple, in Arabidopsis seeds, lipids are stored in cotyledons that show #aredic# and m#s gene expression coding &or isocitrate lyase and #alate synthase, respectively, two 9ey enzymes in the glyoxylate cycle *(astmond and 5raham, "##$). +ight plays an important role in post ger#ination growth, it being observed in #$tants o& Arabidopsis %ic#& that a red$ction in the activity o& isocitrate lyase inhibits lipid breadown and
$nits o& acetylCoA capable o& entering the glycolate cycle" !$gar (s$crose) is the $lti#ate prod$ct o& this process, being the pri#ary &or# in which red$ced C is translocated &ro# the cotyledons to the growing seedling tissues *Taiz and Heiger, $@@$).
strongly red$ces the growth o& hypocotyl (ast#ond et al", +000)" n seedlings, the glyoxylate cycle plays a ey role in growth beca$se it is involved in lipid #etabolis# thro$gh the Joxidation o& &atty acids ('inelstein and >ibson, +00+)" This oxidation prod$ces twoC
protein co#plexes (, , , D) inserted in the inner #itochondrial #e#brane ad on to O +, which acts as a final electron acceptor, finally reduced in the form o& +7 *6ailey/erres and Aoesene9, "##> /weetlove et al", +010)" The electroche#ical potential prod$ced in
"xidati&e posporylation in plants Oxidative phosphorylation (OXPO!) ('ig$re <) is the pathway in which oxidation o& -A. and 'A. +, which are prod$ced d$ring the TCA cycle, occ$rs" ere, the electrons res$lting &ro# oxidation are trans&erred thro$gh
/ource: %uthor based on &eltier and 'ournac *"##") and 6auwe et al. *"#$#). i
e
OXPO! abbreviations: : cytochro#e or -A. dehydrogenase, -.+ , -.+ , -A.(P) dehydrogenase type internal and1 external, respecti vely, : cytochro#e or s$ccinate dehydrogenase, ?K: $bi%$inone, AOX:i alternative oxidase2 : cytochro#e c red$ctase or cytochro#ebc , D: cytochro#e c oxidase or COX, ATPase: ATP synthase, ? or ?CP: $nco$pling protein, PPasa: pyrophosphate synthase"
Chlororespiration abbreviations: OAA: oxaloacetate, P!: photosyste# , PK pool o& plasto%$inone, -dh or -A.(P)PK, -A.(P) dehydrogenase co#plex or -A.(P)plasto%$inone oxidored$ctase, respectively, Cyt b'/(, cytochro#e b'/(, PC: plastocya nin, P!: photosyste# , F
'd: &erredoxin, '-R: &erredoxin -A.P red$ctase" .igure 4+ /(emati( representation o' oxidati&e posporylation 0"5P6"/ 0- and (lororespiration 03+
6+
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the inner #itochondrial #e#brane is the &orce that drives ATP synthesis (/illar et al", +011)" In plants, studies have focused on finding alternative pathways to the conventional OXPO! pathway o& the electron transport chain" 'or exa#ple, the participation o& certain alternative pathways that involve proteins associated with co#plex (Ras#$sson et al", +005) and AOX (/oore et al", +00+) has been proposed ('ig$re <)" owever, nonphosphorylation pathways do not contrib$te to the generation o& the inner#e#brane proton gradient *ernie et al., "##B). To overcome this
deficiency in the proton gradient, plants have a strategy developed &ro# $nco$pling proteins (?CP) e#bedded in the inner #itochondrial #e#brane (!#ith et al", +0052 Arnholdt!ch#itt et al", +006)" ?nco$pling proteins activity can enhance the trans&er o& protons into the #itochondria by controlling the rate o& prod$ction o& s$peroxides, and #ay even have so#e control over the TCA cycle, beca$se increases in the ?CP content can increase the rate o& conversion o& pyr$vate to citrate (!#ith et al", +005)" n both plants and ani#als, once in the #itochondria, -A. and 'A.+ are oxidized in a complex called -A. dehydrogenase or co#plex ('ig$re
enzyme shared between T'% cycle and 72&17/ ('ig$re + and <)" !$ccinate dehydrogenase has di&&erent &$nctions depending on the tiss$e in which it is &o$nd" or example, some influence of /!1 has been reported in leaves with phytochro#e A, which controls the activity o& !. (Plaxton and PodestE, +006)" Co#plexes and D (cytochro#e c red$ctase and cytochro#e c oxidase (COX), respectively) correspond to the OXPO! s$perco#plex, COX being a pri#e OXOPO! ter#inal oxidase (Popov et al", +010)" .espite COX, there is another ter#inal oxidase that is inserted in the inner #itochondrial #e#brane, called alternative oxidase (AOX) ('ig$re <)" s was tho$ght that AOXIs &$nction was to s$pport the trans&er o& electrons when COX was at &$ll capacity (van .ongen et al", +011)" -evertheless, is nown that both AOX and COX co#pete &or electrons, beca$se both are positioned at critical
727&17/ control points *+ambers, $@"). /tudies have el$cidated a cr$cial role o& AOX in protecting against RO! prod$ced d$ring oxidative stress (van .ongen et al", "#$$), and it can also influence mitochondrial adaptability to di&&erent inds o& stress (/oller, +0012 Ras#$sson et al", +00=), even expressing #itochondrial genes in a wide variety o& environ#ents" AOX acts against RO! as &ollows: AOX allows electron trans&er &ro# $bi%$inone (?K) to O +, which high levels o& red$cing agents in the ?K pool can be dissipated thro$gh AOX, th$s avoiding the &or#ation o& RO! (Polidoros et al", +00=)"
%lororespiration n plants, it is possible &or electron transport to O + to occ$r in the presence o& light thro$gh thylaoidal #e#branes o& chloroplasts, via chlororespiration ('ig$re <) (Polidoros et al., "##@), distinct from photorespiration *6ennoun, 1=9+2 Peltier and Co$rnac, +00+) and the /ehler reaction" The &$nction o& this process is to ens$re s$pplies o& ATP and -A.(P) generated by glycolysis &or converting starch into or triose phosphate (.glyceraldehyde phosphate dihydroxyacetone phosphate) *6auwe et al., "#$#> ;aurino and &eterhansel, "#$#). 6oth chloroplasts and #itochondria share si#ilar #echanis#s and control co#ponents, e"g" the electron transport is carried o$t in the #e#brane and shares the sa#e #e#brane co#ponents (cytochro#e, ion! proteins, %$inones and ATPase) *6ennoun, $@"). %lthough there are no exclusive carriers o& -A.(P) in the thylaoidal #e#brane, this #ay be per&or#ed indirectly thro$gh OAA#alate ports which allow the trans port of malate *ig ure ), being oxidized by F
-A. to prod$ce -A. in the chloroplast stro#a
*6ennoun, $@"). The ability to transport reducing agents thro$gh the inner chloroplast #e#brane #eans that it is in co##$nication with the rest o& the cell" There have been st$dies on the i#portance o& environ#ental changes in chlororespiration, with an increase in the activity and expression o& a protein co#plex called -. (ho#ologo$s to co#plex ) (Peltier and Co$rnac, +00+)" This co#plex catalyzes the transfer of electrons from %!*&)1 to plasto%$inones (R$#ea$ et al", +00;)" According to so#e a$thors, this co#plex is ey in chlororespiration beca$se it has an -A. dehydrogenase &$nction in #itochondria" n t$rn, the -dh co#plex reg$lates the proton gradient prod$ced in the stro#a, s$ggesting a role in the control o& oxidative stress prod$ced in the chloroplast stro#a (R$#ea$ et al", +00;)"
Potorespiration ?nlie chlororespiration, photorespiration (also called the C+ cycle) corresponds to an oxidation #echanis# o& C #olec$les (s$ch as rib$lose 1,;diphosphate) and is per&or#ed in three di&&erent organelles: chloroplasts, #itochondria and peroxiso#es (Peltier and Co$rnac, +00+)" This process consists in replacing CO + &or O + during ' fixation in photosynthesis, allowing recycling
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and trans&or#ing the phosphoglycolate (+P>) generated into phosphoglycerate (/a$rino and Peterhansel, +010)" Photorespiration is one o& the #ost i#portant pathways o& carbon #etabolis# in plants, exceeded in its i#portance at the terrestrial level only by photosynthesis" This is beca$se o& the high O+ concentration in the cells co#pared to CO +" Photorespiration can release abo$t +0L o& the CO + that is absorbed d$ring photosynthesis $nder nor#al te#perat$res" owever, it was deter#ined that the a#o$nt and dry o& CO + released co$ld be higher in hot environments *6auwe et al., "#$#> ;aurino and Peterhansel, +010)" The interaction between photorespiration and #itochondrial respiration is generated &ro# an allosteric reac tion in the TCA cyc le using the products of the reaction catalyzed by glycine decarboxylase (>.C) and an interaction between -A. regenerated by the >.C and the electron transport chain
F
*igure 6). The i#portance o& photosynthesis and photorespiration has been observed in tobacco ( )icotiana tabac$m +.) mutants deficient in complex I expression for #itochondrial OXPO!, beca$se the proteins o& co#plex are i#portant &or #aintaining the redox conditions in the cell that enhance photosynthetic efficiency *&eltier and
Co$rnac, +00+2 Plaxton and PodestE, +0062 van .ongen et al", +011)" .un(tions o' plant respiration There is a great deal o& in&or#ation available abo$t #olec$lar and physiological aspects o& plant respiration and its i#portance &or plant growth and develop#ent" owever, there is little in&or#ation abo$t the lin between respiration and ey processes in the s$rvival o& several plant species" -ine processes have been described to tae priority &ro# the energetic point o& view: growth (.$tille$l et al", +00<), nitrate red$ction, sy#biotic - fixation, upta9e of nitrate and other ions by roots *van Iersel and /eymour, "###> Thongo ;?6ou et al., "#$#),
protein t$rnover (Poorter et al", 1==1), #aintenance o& protons gradient *!e Aisser et al., $@@"> 6ouma et al., 1==52 !che$rwater et al", +000), waste #echanis#s and heat prod$ction by alternative pathways (Deen, 1=902 6ouma and !e Aisser, $@@). 5enerally, these processes are associated with two co#ponents o& respiration: growth and #aintenance respiration (ohnson et al", 1==9)" -evertheless, it is possible aggregate a third co#ponent when the correlation between relative growth rate (R>R) and net - $ptae rate (--?R) is not tight (A#thor, +0002 Thornley and Cannell, +000)" >rowth respiration is respiration that prod$ces energy and C seletons &or the synthesis o& new str$ct$res in growing plants (proteins, lipids, organic acids, and str$ct$ral carbohydrates) (Deen, 1=90)" /aintenance respiration is respiration that prod$ces energy &or all processes related to cell$lar #aintenance s$ch as protein t$rnover, #aintenance o& ion gradients and #e#brane potentials in the cell (Penning de Dries et al", 1=752 Penning de Dries, 1=7;)" A #athe#atical expression o& the relationship between these co#ponents o& respiration is: M1N Rr * Rm + cg , R-R + c $ , ))R 1 1 where Rr is root respiration rate *Imol 7+ or CO+ g d ), Rm is respiration rate to prod$ce ATP re%$ired &or #aintenance o& bio#ass, cg is root respiration to prod$ce ATP &or 1 cell$lar co#po$nd synthesis (##ols O + or CO+ g ), R-R 1
1
is the relative growth rate o& roots (#g g d ), c$ is the 1 respiration rate reJuired for maintenance *mol g 1 d ), and --?R is the net - $ptae rate (Deen, 1=90)" The energy re%$ire#ents &or each process depend on the rates associated with the#, which are a&&ected by the species, organ (tiss$e) and environ#ental conditions to which the plants are subjected *+ambers, "##). or exa#ple, 'ig$re 5 shows that yo$ng plants $nder high - conditions allocated only 10L to the #aintenance co#ponent o& root respiration (Poorter et al", 1==1)" On the other hand, the growth co#ponent is an i#portant
!o$rce Poorter et al" (1==1)" .igure 7+ Respiratory (osts as so(iated wit respiration (omponents o' maintenan(e, growt, and ion uptae+
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part o& root respiration (+0L5;L)2 however, the #aBority o& the respiration is devoted to the ion $ptae process (;0L70L) (Poorter et al", 1==1)" n a st$dy in are, #aintenance respiration was the #ost i#portant co#ponent associated with respiration beca$se &$lly grown plants were $sed, which #eant lower R>R and --?R (van der Ger& et al", 1=99)"
val$es o& 1"+ to 1"5 g gl$cose g ./ (0"+ to 0"5 g CO 1 g ./) (Cannell and Thornley, +000)"
Protein t$rnover corresponds to the #aBor &raction o& the #aintenance co#ponent o& respiration" t is partic$larly i#portant when rapid changes occ$r in the environ#ent or d$ring periods o& stress" Githo$t this #echanis# (protein
;"< and 0"9 ##ol O + g ./ &or COX and AOX, respectively, while #aintenance respiration via COX and
t$rnover), the energy re%$ire#ent wo$ld be increased by a high de#and &ro# the plant, so protein t$rnover co$ld eeps the #etabolis# stable in a wide variety o& environ#ents and at all stages o& develop#ent (van der Ger& et al", 1=99)" t is esti#ated that between +L and ;L o& all proteins are replaced daily2 however, there are reports indicating that protein t$rnover in leaves co$ld be as #$ch as +0L daily" !o#e o& the processes associated with protein t$rnover are: biodegradation o& proteins, activation and t$rnover o& a#ino acids, peptide bond &or#ation and posttranslational processes, a#ong others *6ouma et al., $@@B).
Respiration cons$#ed =0L and 60L o& respired C &orthro$gh growth COX and #aintenance, respectively, while AOX cons$#ed 10L and 50L o& available C &or growth and #aintenance respiration, respectively *6ouma, "##E). These results show an interesting e&&ect, beca$se respiration thro$gh '72 varies more in response to -5- than %72 *lorez
!o#e researchers woring $nder di&&erent growth conditions, have correlated #aintenance respiration rates and protein content o& bio#ass (Poorter et al", 1==1)2 th$s, it can be in&erred that protein t$rnover costs are the #ost
"xygen a&aila)ility 'or plant respiration
i#portant costs o& #aintenance respiration" n a co#parative st$dy on roots o& &astgrowing ( Dacty#is g#omerata +.) and slowgrowing (est$ca ovina +.), it was shown that the cost associated with protein t$rnover acco$nted &or between ++L and <
the O+ s$pply &ro# the environ#ent, tiss$e O + having a great influence on the central pathways o& carbohydrate synthesis (/illar et al", 1==9)" n plants, the #aBor external &actors a&&ecting O+ availability are flooding and waterlogging of soil *+iao and +in, "##$).
1
1
esti#ated at approxi#ately +00 ##ol CO + g d (!che$rwater et al", +000)" Another portion o& the costs associated with #aintenance are dedicated to reg$lating the ionic gradient, also nown as the cellIs os#otic potential, where the costs o& #aintaining the ionic gradient are 1
1
approxi#ately 500 ##ol CO+ g d
(A#thor, +000)"
Otherwise, the growth co#ponent is $s$ally expressed in
+
C$rrently, other st$dies &oc$s on the contrib$tions that ter#inal oxidases (COX and AOX) sho$ld have on the growth and #aintenance co#ponents o& plant respiration" n Arabidopsis plants, Cannell and Thornley (+000) esti#ated the constr$ction cost o& lea& tiss$es, which corresponded to 1
1 1
AOX was 15"< and = n#ol O + g s . /imilar values were found by lorez/arasa et al" (+007) in the sa#e species"
!arasa et al", +007)" Ghen R>R is low (decreasing or not the respiration) AOX activity is increased, allowing it to #aintain the redox state o& the $bi%$inone pool to inhibit -7/ *lorez/arasa et al., "##K). A #aBor &actor that a&&ects plant respiration is O + depletion, in the rhizosphere or directly in tissues. The 7 + availability in tiss$es and cells depends on the plantIs age and especially on
?nder these conditions we can disting$ish three broad categories o& oxygen stat$s ind$ced by water: nor#oxia, hypoxia, and anoxia (Table 1)" xcess water in soil decreases the O+ di&&$sion rate, beca$se the di&&$sion o& 5
O+ is 10 times slower in water than in air *+iao and +in, "##$>
C $nits (c g &ro# %$ation M1N), corresponding to new
b$t also the di&&$sion o& several other gases s$ch as CO+ and
bio#ass per $nit o& gl$cose (Penning de Dries, 1=7;)" /ost plant cg val$es are between 0"7 and 0"9, e%$ivalent to the
ethylene (Gegner, +010)" t is i#portant to consider that low O+ availability in cells can even occ$r in so#e sit$ations
cost o& constr$cting the gl$cose re%$ire#ent, with
$nder nor#oxia, d$e #ainly to a high resistance
Ta)le 1+ #es(ription o' tree states o'2 " deficiency due to excess water. -or#oxia 1
Aerobic Oxidative phosphorylation (OXPO!) pathway 1 L #0 mol %T& mol glucose consumed ormal
/etabolis# 1 -A.F regeneration 1
ATP prod$ction
1
ATP and8or A.P cell$lar content +
Oxygen content +
1
9"09"; #g O+ +
+
+1
ypoxia
Anoxia
nhancedanaerobic Alcoholic and lactic &er#entation pathways !ependent on species +ow%T& 1";6"0 #g O+ +
1
Anaerobic Alcoholic and lactic &er#entation pathways 1 L B mol %T& mol o& gl$cose cons$#ed +ow%T&andhigh%!& 1
0 #g O+ +
+
9"; #g O + Q +1L O M "K# ; 7 Q 100L O saturation. The oxygen content defined for each condition is not the same for all species. 1
+
/oore et al" (+00+)2 !weetlove et al" (+010)" /oore et
al" (+00+)2 Arnholdt!ch#itt et al" (+006)"
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to O+ di&&$sion between di&&erent plant tiss$es (>ibbs and >reen way, +00<) s$ch as roots and ste# s (van .ongen et al", +011)" !o#eti#es, to red$ce the anaerobic state in shoots, roots reg$late &re%$ency o& absorption (Ar#strong et al., $@@B> Habalza et al., "##@) and oxygen consumption
(/anc$so and /arras, +006)" /orphological adaptations also play a ey s$pporting role in pro#oting the O + flux from the roots through the rest of the plant, e.g. aerenchy#a &or#ation d$e to ind$ction by ethylene (>reenway and >ibbs, +00<)" One o& the #ain e&&ects o& anaerobiosis on #etabolis# is a decreased adenylate energy charge (AC), which also red$ces the ATP:A.P ratio (.rew et al", +000)" ?nder hypoxic conditions the TCA cycle pathway gives more flexibility to the overall metabolism *Table $). 'or instance, in ot$s aponic$s, it was shown that alanine a#inotrans&erase (AlaAT) generates a lin between glycolysis and the TCA cycle thro$gh the conversion o& + oxogl$tarate to s$ccinate" This generates -A. that is $sed in the trans&or#ation o& OAA into #alate2 together with s$ccinate CoA ligase, both contrib$te to the generation of %T& under conditions of oxygen deficit *5eigenberger, "##> 6ailey/erres and Aoesene9, "##). /oreover, glycolysis is a&&ected when O + concentration &alls below 1";+"0 #g O + +
1
in the b$l sol$tion
(hypoxia)" This decreases glycolysis and increases the activities of enzymes involved in fermentation *+i et al., "#$#). In maize subjected to hypoxia, &!' activity increases ;to=&old co#pared to that $nder nor#al conditions (>$pta et al", +00=)" t is nown that there are two #aBor control points &or electron trans&er $nder oxygen deficit, corresponding to %72 and '72. /ome studies suggest that the response to oxygen deficiency in roots is driven by the ter#inal oxidation o& respiration (*ennedy et al", 1==+)" ?nder so#e conditions, when
the availability o& O + in roots is decreased, adaptation to stress may occur through two strategies> the first is a decrease in ATP cons$#ption which leads to a #etabolic crisis at the cell$lar level (ga#berdiev et al", +010), and the second is an increase in the glycolytic flux *;ancuso and /arras, +006)" The latter is called the Paste$r e&&ect (>ibbs et al", +000), consisting o& a progressive acceleration in carbohydrate #etabolis# that allows the plants to #aintain their energy level, especially d$ring the early phase of acclimation to oxygen deficiency *Turner,
1=;12 >reenway and >ibbs, +00<2 Ca#achoPereira et al",%lthough +00=2 Gegner, many +010)" authors emphasize the importance of the N&asteur effectO in acclimatization processes to compensate for the energy inefficiency caused by OXPO! inhibition (>ibbs and >reenway, +00<2 $ang et al", +009), this can only generate ATP at abo$t <7";L o& the rate prod$ced in tiss$es $nder opti#al oxygen conditions (>eigenberger, +00<)" The O + is a molecule that participates as a final electron acceptor in the transport chain co#plexes (>ibbs and >reenway, +00<)2 there&ore, when oxygen availability decreases dramatically in the rhizosphere (anoxia, Table 1), OXPO! is inactivated (/oller, +001) and terminal oxidase *'72) is inhibited *+iao and +in,
+0012 >reenway and >ibbs, +00<2 /anc$so and /arras, +0062 /aillo$x et al", +007)" ?nder these conditions, plants have developed alternative pathways to aerobic respiration in order to #aintain glycolysis thro$gh the F
regeneration o& -A. (>$pta et al", +00=) and th$s obtain the energy needed to #aintain ey processes o& #etabolis# s$ch as #e#brane integrity and th$s ion selectivity (Tadege et al", 1===), protein synthesis and t$rnover and reg$lation o& cytosolic p, a#ong others *6lo9hina et al., "##). These alternative pathways
are nown as &er#entations"
!o$rce: A$thor based on >$pta et al" (+00=)" OAA: Oxaloacetate" .igure 8+ Representation o' anaero)i( respiration+ Green )oxes and arrows sow te la(ti( a(id and al(ooli( 'ermentation+ Purple )oxes and arrows sow te (y(le tat in&ol&es alanine+
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CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 75
Three &er#entative pathways are nown (>reenway and >ibbs, +00<) that are active $nder conditions o& oxygen deficiency *igure E): alcoholic fermentation, lactic &er#entation (!o$sa and !ode, +00+) and the alanine pathway> the last one is specific to plants and its final product is alanine from glutamate and the pyruvate reaction *Tadege et al., $@@@). There are also other final prod$cts o& &er#entation s$ch as s$ccinate, #alate, and 4aminobutyric acid *!ennis et al., "###). 'ro# the energy point o& view, &er#entative pathways can prod$ce between ;L and 10L o& the ATP per #ole
&er#entation, where the absence o& oxygen wo$ld not be responsible for inducing enzymes such as &'! and %!1, is highly desirable (*ennedy et al", 1==+2 Rah#an
of glucose oxidized in aerobic respiration *!rew, $@@K> !o$sa and !ode, +00+)" n the roots o& grapevines, &or exa#ple, $nder nor#al conditions abo$t ++"; n#ol ATP 1 g &resh weight are obtained, b$t in anoxia only + n#ol 1 ATP g &resh weight are prod$ced (>eigenberger, +00<)" The activation o& a &er#entation pathway is $s$ally initiated when an anaerobic event occ$rs (Tadege et al., $@@@> 6ailey/erres and Aoesene9, "##)> later, the pyr$vate is red$ced to lactic acid by lactate dehydrogenase *+!1) in the cell?s cytoplasm *Tadege et al., $@@@). +!1 acts at a p1 near K.B *3ato oguchi and /oro$#a, +007) and is responsible &or #aintaining the redox balance witho$t the loss o& C associated with alcoholic &er#entation" owever, the acc$#$lation of this enzyme leads to a decrease in cytosolic p1 to levels between 6"5 and 6"9 (Tadege et al", 1===)" %cidification of the cytoplasm inactivates +!1 and activates pyr$vate decarboxylase (P.C) (Roberts et al", 1=95), which decarboxylates pyr$vate and &or#s acetaldehyde, which in turn is finally reduced to ethanol by alcohol dehydrogenase (A.) ('elle, +00;)" n 3itis riparia /ichx" and 3. r$pestri !cheele plants s$bBected to anoxia d$ring +5 h, both species showed high levels o& ethanol as the principal co#ponent o& &er#entation, 1 &resh weight (3. riparia yielding ""E and $KE Imol g and 3. r$pestri, respectively) at +0 h o& treat#ent" ?nder 1 normal conditions the level was B# Imol g &resh weight (Tadege et al", 1===2 *ato-og$chi and /oro$#a, +007)" The i#portance o& alcoholic &er#entation in tolerance to oxygen deficiency has also been shown in rice, where the response o& di&&erent c$ltivars to 59 h o& anoxia has been de#onstrated" This st$dy showed that at the end of the treatment +!1 activity was insignificant. n contrast, PC. and A. activities were, on average, were ind$ced = &old co#pared with their stat$s in the sa#e coleoptiles $nder nor#al conditions (/anc$so and /arras, +006)" in Arabidopsis #$tants has indicated val$ation that overexpression o& PC. and A. pro#otes stress tolerance during oxygen deficiency, because thecarbon flux is controlled through alcoholic fermentation and thro$gh the lactate and alanine pathways (*ato -og$chi and /oro$#a, +007)" -evertheless, additional in&or#ation abo$t the special &eat$res associated with fermentative pathways, and specifically alcoholic
exist 9ey enzymes as control points:two hexo9inase and participating pyruvate 9inase. 6oth enzymes can control glycolysis not only in #itochondria b$t also at a posttranslational level"
et al", +0012 s#ond et al", +00<2 *$rsteiner et al", +00<)" %"!%9$/I"!/
Plant respiration is a highly dyna#ic process, beca$se the pathways involved present a high capacity to adapt to di&&erent environ#ental conditions" >lycolysis is one o& these pathways2 controlling several reactions in which
The tricarboxylic acid (TCA) cycle has a strong influence on respiration metabolism through enzymatic control" The TCA cycle is not only involved in reg$lating the respiration rate, b$t also participates in the synthesis o& inter#ediates o& the sa#e cycle s$ch as isocitrate, #alate, and s$ccinate" n t$rn, the TCA cycle reg$lates so#e ey processes in photosynthetic #etabolis# s$ch as CO+ assi#ilation" The existence o& alternative pathways s$ch as 5%6% and the glyoxylate cycle gives the T'% cycle &$rther plasticity in adapting to environ#ental changes" There is little in&or#ation with respect to the lin between energy &or respiration and processes i#portant &or a plant #etabolis#" Co#ponents o& respiration associated with growth and ion $ptae are highly dependent on &actors s$ch as the species, plant organ and environ#ental conditions a&&ecting the relative growth rate and net - upta9e rate coefficients. The maintenance component also responds &avorably to rapid changes in the environ#ent, d$e to its high capacity to #odi&y protein t$rnover in the cells" A plantIs capacity to tolerate anaerobic conditions not only relates to bioche#ical properties o& the roots, b$t also the plantIs capacity to transport O + transport &ro#
oxygenated organs to anoxic organs. 6oth glycolysis and &er#entation are principal #echanis#s o& energy #aintenance in the cells and their &$nction is i#portant in a plantIs tolerance to O+ deficiency. Plant respiration is considered a principal #echanis# o& ecosyste# #aintain on the planet" There&ore, it is i#portant that new research sho$ld &oc$s on predicting the i#pact that cli#ate change will have on respiratory #etabolis#, especially at the &$nctional and geno#ic levels" -%!"W9E#GEME!T/
Pe than9 the 'entro de (studios %vanzados en 'r$tic$lt$ra (CA') and the CO-CT Regional proBect -#I$##$ for financing this review. The authors wish to than to pro&essor Ti# Col#er &or critical review o& the #an$script"
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9ITER-T$RE %ITE# A#thor, "!" +000" The /cCreede GitPenning de DriesThornley -espiration &aradigms: # Qears +ater. %nnals of 6otany 0:$"#. %rmstrong, P., ;.(. /trange, /. 'ringle, and &.;. 6ec9ett. $@@B.
/icroelectrode and #odelling st$dy o& oxygen distrib$tion in roots. %nnals of 6otany KB:"K"@@. %rnholdt/chmitt, 6., <.1. 'osta, and !.. de ;elo. "##0. %72 a functional mar9er for efficient cell reprogramming under stressR
Trends in Plant !cience 11:+91+97" %t9in, 7.3., <.-. (vans, ;.'. 6all, 1. +ambers, and T.+. &ons. "###. +eaf respiration of snow gum in the light and dar" nteractions between te#perat$re and irradiance" Plant Physiology 1++:=1;=+5" Atin, O"*", "R" vans, and *" !iebe" 1==9" Relationship between the inhibition o& lea& respiration by light and enhance#ent o& lea& dar respiration &ollowing light treat#ent" A$stralian o$rnal o& Plant Physiology +;:5<755<" Atin, O", A" /illar, P" >ardestrS#, and ." .ay" +005" Photosynthesis, carbohydrate #etabolis# and respiration in leaves o& higher plants. p. $E$KE. In +eegood, -., T. /har9ey, and /. 'aemmerer
(eds") Photosynthesis" !pringer, .ordrecht, The -etherlands" %urisano, ., %. 6ertani, and -. -eggiani. $@@E. Involvement of calci$# and cal#od$lin in protein and a#ino acid #etabolis# in rice roots $nder anoxia" Plant and Cell Physiology <6:1;+;1;+="
%zama, 3., /. %be, 1. /ugimoto, and (. !avies. "##. +ysinecontaining proteins in maize endosperm: % major contribution &ro# cytoseletonassociated carbohydrate metabolizing enzymes. &lanta "$K:0"0. 6ailey/erres, <., and +. Aoesene9. "##. looding stress: Accli#ations and genetic diversity" Ann$al Review o& Plant 6iology E@:$@. 6auwe, 1., ;. 1agemann, and %.-. ernie. "#$#. &hotorespiration: players, partners and srcin" Trends in Plant !cience 1;:<<0<<6" 6ennoun, &. $@". (vidence for a respiratory chain in the chloroplast.
Proceedings o& the -ational Acade#y o& !ciences o& ?!A 7=:5<;+5<;6" 6ernstein, ., %. (shel, and T. 6eec9man. "#$. (ffects of salinity on root growth. '-' &ress, 6oca -aton, lorida, 8/%. 6lo9hina, 7., (. Airolainen, and 3.A. agerstedt. "##. %ntioxidants, oxidative da#age and oxygen deprivation stress: A review" Annalsof 6otany @$:$K@$@B. 6ouch=, ., and 1. romm. "##B. 5%6% in plants: just a metaboliteR
Trends in Plant !cience =:11011;" 6ouma, T. "##E. 8nderstanding plant respiration: /eparating respiratory co#ponents vers$s a processbased approach" p" 177 $@B. In +ambers, 1., and ;. -ibas'arbo *eds.) &lant respiration.
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A" >alina" +00=" Reactive oxygen species prod$ction by potato t$ber #itochondria is #od$lated by #itochondrially bo$nd hexoinase activity" Plant Physiology 15=:10==1110" Cannell, /">"R", and ""/" Thornley" +000" /odelling the co#ponents o& plant respiration: !o#e g$iding principles" Annals of 6otany E:BEEB. de /ousa, '.%.., and +. /ode9. "##. %lanine metabolism and alanine a#inotrans&erase activity in soybean ( -#ycine ma ) d$ring hypoxia o& the root syste# and s$bse%$ent ret$rn to nor#oxia"
(nvironmental and (xperimental 6otany E#:$.
!e Aisser, -., '.<.T. /pitters, and T.<. 6ouma. $@@". (nergy costs o& protein t$rnover: Theoretical calc$lation and experi#ental esti#ation &ro# regression o& respiration on protein concentration of fullgrown leaves. p. B@E#. In +ambers, 1., +.1.P. van der Plas (eds") /olec$lar, bioche#ical and physiological aspects o& plant respiration. /&6 %cademic &ublishing, %msterdam, The -etherlands" .ennis, "!", R" .ol&er$s, /" llis, /" Rah#an, " G$, '"?" oeren, et al" +000" /olec$lar strategies &or i#proving waterlogging tolerance in plants.
&lant &hysiology and &lant ;olecular 6iology B:"""E#. .rew, /"C", C"" e, and P"G" /organ" +000" Progra##ed cell death aerenchy#a &or#ation in roots" Trends in Plant !cienceand ;:1+<1+7" .$tille$l, C", !" .riscoll, >" Cornic, R" .e Paepe, C"" 'oyer, and >" -octor" +00<" '$nctional #itochondrial co#plex s re%$ired by tobacco leaves &or opti#al photosynthetic per&or#ance in photorespiratory conditions and d$ring transients" Plant Physiology 1<1:+65+7;" (astmond, &.<., A. 5ermain, &.-. +ange, <.1. 6ryce, /.;. /mith, and "A" >raha#" +000" Postger#inative growth and lipid catabolis# in oilseeds lacing the glyoxylate cycle" Proceedings o& the -ational Acade#y o& !ciences o& ?nited !tates o& A#erica =7:;66=;675" ast#ond, P"", and "A" >raha#" +001" Reexa#ining the role o& the glyoxylate cycle in oilseeds" Trends in Plant !cience 6:7+79" elle, 1.1. "##E. p1 regulation in anoxic plants. %nnals of 6otany =6:;1=;<+" ernie, %.-., . 'arrari, and +.<. /weetlove. "##B. -espiratory #etabolis#: >lycolys is, the TCA cycle and #itochondrial electron transport. 'urrent 7pinion in &lant 6iology K:"EB"0$. in9elstein, -., and /. 5ibson. "##". %6% and sugar
interactions regulating development: 'rosstal9 or voices in a crowdR 'urrent 7pinion in &lant 6iology E:"0". lorez/arasa, I.!., T.<. 6ouma, 1. ;edrano, <. %zcon6ieto, and ;. RibasCarbo" +007" Contrib$tio n o& the cytochro#e and alternative pathways to growth respiration and #aintenance respiration in Arabidopsis tha#iana " Physiologia Plantar$# 1+=:15<1;1"
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Reg$lation o& alcoholic &er#entation in coleoptiles o& two rice c$ltivars di&&ering in tolerance to anoxia" o$rnal o& xperi#ental 6otany E$:KEK@0. 5ieg=, &., <.+. 1eazlewood, 8. -oessnerTunali, %.1. ;illar, %.-. ernie, '.<. +eaver, et al. "##. (nzymes of glycolysis are &$nctionally associated with the #itochondrion in Arabidopsis cells" The Plant Cell 1;:+150+1;1" >reenway, ", and " >ibbs" +00<" Review: /echanis#s o& anoxia tolerance in plants" " nergy re%$ire#ents &or #aintenance and energy distrib$tion to essential processes" '$nctional Plant 6iology #:@@@$#0. 5upta, 3.<., %. Habalza, and <.T. Aan !ongen. "##@. -egulation of respiration when the oxygen availability changes" Physiologia Plantar$# 1<7:<9<<=1" achiya, T", " Terashi#a, and *" -og$chi" +007" ncrease in respiratory cost at high growth te#perat$re is attrib$ted to high protein t$rnover cost in "et$nia hybrida petals" Plant, Cell and nviron#ent <0:1+6=1+9<" 1ajirezaei, ;.-., /. 6iemelt, ;. &eis9er, %. +ytovchen9o, %.-. ernie, and 8. /onnewald. "##0. The influence of cytosolic phosphorylating glyceraldehyde <phosphate dehydrogenase (>APC) on potato t$ber #etabolis#" o$ rnal o& xperi#ental
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TP speci&ic s$ccinylCoA synthetases in multicellular eu9aryotes. The a##a acid *5%6%) and plant to stress. 'ritical a#inob$tyric -eviews in &lant
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;illar, %.1., <. Phelan, 3.+. /oole, and !.%. !ay. "#$$. 7rganization and regulation of mitochondrial respirat ion in plants. %nnual -eview of &lant 6iology 0":K@$#B. /oller, "/" +001" Plant #itochondria and oxidative stress: lectron transport, -A.P t$rnover, and #etabolis# o& reactive oxygen species" Ann$al Review o& Plant Physiology and Plant /olec$lar
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C$##ings !an 'rancisco, Cali&ornia, ?!A" Teusin9, 6., <. P$blishing, &assarge, '.%. -eijenga, (. (sgalhado, '.'. van der GeiBden, /" !chepper, et al" +000" Can yeast glycolysis be $nderstood in ter#s o& in vitro 9inetics of the constituent enzymesR Testing biochemistry. (uropean ?!T +01;
