Review Article The Dormancy Marker DRM1/ARP Associated ...Dormancy but a Broader Role In Planta...

Hindawi Publishing CorporationDevelopmental Biology JournalVolume 2013 Article ID 632524 12 pageshttpdxdoiorg1011552013632524

Review ArticleThe Dormancy Marker DRM1ARP Associated withDormancy but a Broader Role In Planta

Georgina M Rae12 Karine David2 and Marion Wood1

1 The New Zealand Institute for Plant amp Food Research Limited Mt Albert Private Bag 92169 Auckland Mail CentreAuckland 1142 New Zealand

2 Plant Molecular Sciences School of Biological Sciences University of Auckland Private Bag 92019 Auckland Mail CentreAuckland 1142 New Zealand

Correspondence should be addressed to Georgina M Rae georginaraeplantandfoodconz

Received 28 February 2013 Revised 15 May 2013 Accepted 16 May 2013

Academic Editor M Pisano

Copyright copy 2013 Georgina M Rae et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Plants must carefully regulate their development in order to survive a wide range of conditions Of particular importance to this isdormancy release deciding when to grow andwhen not to given these varying conditions In order to better understand the growthrelease mechanism of dormant tissue at the molecular and physiological levels molecular markers can be used One gene familythat has a long association with dormancy which is routinely used as a marker for dormancy release is DRM1ARP (dormancy-associated gene-1auxin-repressed protein)This plant-specific gene family has high sequence identity at the protein level throughoutseveral plant species but its function in planta remains undetermined This review brings together and critically analyzes findingson the DRM1ARP family from a number of species We focus on the relevance of this gene as a molecular marker for dormancyraising questions of what its role might actually be in the plant

1 Introduction

Plants are sessile therefore a number of mechanisms areelegantly managed in the plant to ensure its survival andoptimisation in its given setting Integral to this is the tem-poral and spatial determination of growth in relation to thesurroundingsThis growthmay be vegetative such as axillarybudbreak and branch development or floral including flowerand fruit development To achieve this cell division cellelongation or a combination of the two has been shown toplay a pivotal role in plant growth regulation

Dormancy is a means of ensuring a plantrsquos long-term sur-vival and is defined as the ldquotransitory delay of visible growththat occurs in plant meristematic tissuesrdquo [1] An exampleof this occurs in perennials over winter When temperaturesare low and daylight hours are limited plants protect them-selves by ceasing growth waiting for the more favourableconditions of spring in which they focus their resources ongrowing and reproducing As such the key decisions aroundwhen to release dormant tissue from dormancy (dormancy

releaseshoot outgrowthshoot branching) are an importantmechanism for plant biologists to understand

Both perennial and annual plants (eg Arabidopsis) alsoundergo a type of dormancy known as apical dominanceor paradormancy where endogenous signalshormones fromthe apical bud are received by lower axillary meristemspreventing their bud outgrowth This phenomenon was firstdescribed in 1934 [2] when it was shown that axillary budsof decapitated plants were released from dormancy due to alack of auxin flow down the stem Since then the interactionsbetween auxin and other hormones including cytokinin(growth promoting) and strigolactone (branching inhibition)have been studied in-depth in order to better understand thecomplex cross-talk which is controlling this process [3]

Mutant lines exhibiting hyperbranching phenotypes havebeen integral to these dormancy release studies Theseincluded characterisation of the MAXCCDRMS pathwayinvolved in strigolactone biosynthesis and perception (re-viewed by Seto et al [4]) and more recently additionalhyperbranching mutants the bud-specific dormancy release

2 Developmental Biology Journal

signal integrator brc1tbl1 have also been studied in orderelucidate alternate pathways involved in this critical processThese studies relied heavily on the use of a genetic marker fordormancy statusmdashdormancy-associated gene 1 (DRM1)auxinrepressed protein (ARP) This review will present literatureassociated with DRM1ARP from a number of species (sum-marised in Table 1) and will discuss the relevance of usingDRM1ARP as a molecular marker for dormant tissues

2 DRM1ARP and Dormancy

The first studied member of the DRM1ARP gene familywhose transcript expression was linked with dormancy phys-iology PsDRM (dormancy-associated gene)-1 was isolatedfromdifferential display performedwith cDNA libraries fromdormant and growing axillary buds of pea To consider therelationship between expression of this gene and axillarybud dormancy Stafstrom et al [5] decapitated Alaska peaplants By removing the apical buds of the pea plants thebud can be released from paradormancy (apical dominance)allowing outgrowth of the axillary buds (Figure 1) PsDRM1expression was analysed by northern blot in the bud atvarious time points after decapitation and revealed that uponrelease of dormancy PsDRM1 levels decreased 20-fold witha concomitant increase in the expression of the cell cyclemarker gene PsRPL27 [5]

Two homologues to PsDRM1 have been identified inArabidopsisAtDRM1 (At1g28330) and AtDRM2 (At2g33830formally known as AtDRM1-homologue) As in pea a decap-itation was conducted in Arabidopsis showing that AtDRM1and AtDRM2 expression levels decreased with the release ofparadormancy [6] Subsequent expression levels increasedfrom 24 h after decapitation due to a putative apical dom-inance from the primary axillary outgrowth leading toparadormancy in the lower buds

Dormancy release experiments performedwithAdDRM1the DRM1ARP homologue in Actinidia deliciosa (kiwifruit)using hydrogen cyanamide (commercially available asHiCane) as a dormancy release agent show the same expres-sion profiles [7] Treatment with hydrogen cyanamide wasused to release the apical buds from endodormancy (com-pared with decapitation initiating release of apical budsfrom paradormancy in pea and Arabidopsis) Upon releaseof bud dormancy the characteristic decrease in AdDRM1expression was seen In the same experiment the expressionof AdCDKB (cyclin-dependant protein kinase B) a markerfor growth from kiwifruit was assessed Cyclin-dependentkinases (CDKs) are known to be involved in the reinitiation ofcell cycle progression through the G

1-S phase transition [8]

As AdDRM1 levels decrease AdCDKB expression increases[7]

Further evidence of an association of DRM1ARP tran-scripts with periods of dormancy is seen in PsARP (Paeo-nia suffruticosa auxin-repressed protein) a gene identifiedas being associated with the release of dormant buds oftree peony PsARP showed a sharp increase prior to bud breakand then dropped to low levels as the buds grew [9]

In most cases increases in DRM1ARP expression areassociated with reduced branching phenotypes phyb [10] tin

Dormant axillary buds Buds released from Axillary bud outgrowthdormancy

SAM

Figure 1The ldquodecapitation experimentrdquo used by Stafstrom et al [5]to induce release of dormancy

[11] andCHR12OX [12] and decreases inDRM1ARP expres-sion are associated with increased branching phenotypesaxr1-12 [13] max2 [13] and chr12 [12] (Table 2) HoweverDRM1ARP has also been used as a marker for dormancy inArabidopsis in studies of Teosinte branched 1-like or branched1 (TBL1 or BRC1) [13] with less dependability Results showedthat a reduction in mRNA expression of DRM1ARP was notrequired for bud outgrowth leading to the conclusion at thetime that DRM1ARP was probably acting upstream of TBL1[13] AlternativelyDRM1ARP could be acting independentlyofTBL1 In the same study therewas no change inDRM1ARPtranscript levels in hyperbranching 35SYUCCA where youmay anticipate a reduction in expression providing furtherevidence that DRM1ARP may not be playing a role specifi-cally in holding back bud outgrowth

These findings weaken the argument for DRM1ARP asa molecular marker for dormancy in axillary buds Alterna-tively these data suggest that DRM1ARP is playing a roleas an integrator only under a subset of specific dormancy-related conditions

3 The DRM1ARP Protein Family

Database searches show that theDRM1ARP family is uniqueto plants with homologues found in both monocotyledonsandDicotyledons [25]Multiple protein sequence alignmentsshow high conservation of the DRM1ARP protein prod-uct with two domains clearly identifiable at the amino-terminus and at the carboxy-terminus [7 25] This highconservation across species and indeedmonocotyledons andDicotyledons suggests a potential importance of the actionof this protein in the normal development and physiologyof plants Moreover the protein product is conserved inits size with all 11 species analysed by Park and Han [25]between 11 and 14 kDa (between 109 and 126 amino acidresidues) GFP fusion constructs of EuNOD-ARP1 (EuNOD-ARP1 Elaeagnus umbellata nodule auxin-repressed proteingene 1) a DRM1ARP homologue in the ornamental shrubE umbellata (Japanese silverberry Autumn-Olive) as wellas GFP fusion constructs of Brassica rapa DRM1 and ARP1suggest that it is cytosol-localised [16 18] However in silico

Developmental Biology Journal 3

Table1Summaryof

thec

haracteristicsa

ndpu

tativ

efun

ctionof

know

nDRM

1ARP

family

mem

bers

Species

Protein

identifi

erGenen

ame

Possiblefunctio

nPredicted

proteinleng

th(aa)

Predicted

proteinsiz

e(kD)

PredictedpI

Predicted

extin

ction

coeffi

cient

References

Actin

idiadeliciosa

FG458205

AdeDRM

1ID

Ad

DRM

1Axillary

buddo

rmancy

maintenance

andgrow

threpressio

nin

maturefruit

115

12722

1058

19480

Woo

detal2013

[7]

Arabidopsis

thaliana

NP001154378

AtDRM

1Axillary

buddo

rmancy

maintenance

andleafmaturation

122

13406

1071

19480

Tatematsu

etal

2005

[6]

NP850220

AtDRM

2Axillary

buddo

rmancy

maintenance

108

11500

1032

19480

Arachish

ypogaea

AAZ2

0292

AhDRM

1Droug

htstr

essrespo

nse

121

13459

1019

22460

Govindetal

2009

[14]

Brassicaoleracea

AAL6

74436

BoDRM

1Germinationin

subo

ptim

alcond

ition

s105

11352

1010

19480

Soedae

tal2005

[15]

Brassicarapa

ACQ90305

AAO

32054

BrDRM

1BrARP

1

Preventio

nof

germ

ination

preventio

nof

hypo

cotylelong

ation

temperature

andsaltstr

essrespo

nse

128

108

14035

11651

935

1010

18115

19480

Leee

tal2013

[16]

Capsicu

mannu

umAAR8

38881

CaARP

1Coldandsaltstr

essrespo

nse

Onlypartial

available

Hwangetal

2005

[17]

Elaeagnu

sumbellata

AAC

62104

EuNOD-ARP

1Pathogen

respon

sein

root

nodu

les

120

12985

1026

19480

Kim

etal2007

[18]

Fragariaxananassa

Q05349

Fa120582SA

R5Growth

repressio

nin

maturefruit

111

12416

969

19480

Redd

yandPo

ovaiah

1990

[19]

Malus

xdomestica

AAA71994

MdA

P1Growth

repressio

nin

maturefruit

11913060

1001

19480

Leee

tal1993

[20]

Nicotia

nabenthamiana

GW691612

NbD

RM3

PTIimmun

ity127

13623

1036

16960

Chakravarthy

etal

2010

[21]

Nicotia

natabacum

AAO

21304

NtAR

PL11

Growth

repressio

nin

maturep

ollen

andflo

wers

137

14636

1139

20970

Steinere

tal

2003

[22]

Paeoniasuffrutico

saABW

74471

PsAR

PAxillary

buddo

rmancy

maintenance

126

13725

1039

20970

Huang

etal2008

[9]

Pisum

sativ

umAAB8

4193

PsDRM

1Bu

ddo

rmancy

maintenance

and

grow

threpressio

nin

maturetissues

111

12284

1026

19480

Stafstr

om2000

[23]

Stafstr

ometal1998

[5]


Table1Con

tinued

Species

Protein

identifi

erGenen

ame

Possiblefunctio

nPredicted

proteinleng

th(aa)

Predicted

proteinsiz

e(kD)

PredictedpI

Predicted

extin

ction

coeffi

cient

References

Pyrusp

yrifolia

AGG19165

PpAR

P1Growth

repressio

nin

maturefruit

11612631

1026

19480

Shietal2013

[24]

AGG19166

PpAR

P2139

14273

1058

9970

Robiniapseudoacacia

AAG

33924

RpAR

PElon

gatio

nrepressio

nin

hypo

cotyls

115

12641

1022

19480

Park

andHan

2003

[25]

Solanu

mlyc

opersicum

ABH

07900

SlDRM

1Growth

repressio

nin

ldquodormantrdquo

ovariesp

riortofruitset

123

13442

1011

20970

Vriezenetal

2008

[26]


Table 2 Transcript expression profiles of DRM1ARP family members in characterised mutants

Species Mutant Mutant phenotypeTranscript

expression profilein mutant cfWT

Correlation between DRM1ARPexpression and reduced

branchingenhanced dormancyReference

Arabidopsis thaliana phyb Reduced branchinghyperelongation uarr y Finlayson et al

2010 [10]

Arabidopsis thaliana tbl1brc1 Highly branched mutant mdash n Finlayson2007 [13]

Arabidopsis thaliana axr1-12 Highly branched mutant darr (buds) y Finlayson2007 [13]

Arabidopsis thaliana max2 Highly branched mutant darr (buds) y Finlayson2007 [13]

Arabidopsis thaliana 35SYUCCA Reduced branching mdash n Finlayson2007 [13]

Wheat(Triticum aestivum) tin Reduced

tilleringbranching uarr y Kebrom et al2012 [11]

Sorghum(Sorghum bicolor) phyb-1 Reduced branching uarr y

Kebrom et al2006 [27]Kebrom et al2010 [28]

Arabidopsis thaliana chr12Reduced growth arrestwhen exposed to moderatestress

darr Y Mlynarova et al2007 [12]

Arabidopsis thaliana CHR12OX

Growth arrest of normallyactive primary buds andreduced growth of primaryshoot only uponperception of stressconditions

uarr Y Mlynarova et al2007 [12]

prediction shows AtDRM1 in the nucleus and mitochondriapossibly suggesting differing roles for family members fromdifferent species No characterised localisation signals orDNA-binding domains are found in the protein sequenceAdditionally the PFAMmotif (PF05564) ldquodormancy-auxin-associated proteinrdquo represents almost the entire proteinleaving few hints on the role of this protein in planta

Recently evidence has emerged for DRM1ARP familymembers as intrinsically disordered proteins (IDPs) [7]IDPs found in plants and animals have a large proportionof their sequence yielding no fixed tertiary structure yetstill providing some biological function [29] Signal trans-duction and transcriptional regulation are key processeswithin which structural disorder is prominent [30 31] Awell-characterised example of IDPs in the plant kingdomis the late embryogenesis abundant (LEA) class of proteinsinvolved in abiotic stress tolerance [32 33] as chaperones forother stress response genes [34ndash36] ERD10 and ERD14 (earlyresponse to dehydration) aremembers of the dehydrin type ofLEA proteins shown to be both intrinsically disordered and

responding to high salinity drought and low temperaturestresses in Arabidopsis [36] Similarly a (LEA)-like phos-phoprotein (CDeT11-24) whose expression is associated withperiods of dessication has been identified in the resurrectionplant Craterostigma plantagineum [37] Indeed with thesefindings in mind DRM1ARP family members may haveroles in chaperoning proteins critical to the no-growth phasein tissues

Despite the high degree of conservation across speciesthe biological significance of the DRM1ARP protein familyremains unknown

4 Potential Role of DRM1ARP in theGrowthNo-Growth Decision outside ofMeristematic Tissues

Despite being a commonly used marker for dormancyDRM1ARP is expressed in tissues other than dormant axil-lary buds with high expression often localised to nongrowingtissues


Fruit development is an example of the growthno-growth homeostasis in floral tissues (cf vegetative tissues)and as such provides further evidence ofDRM1ARPrsquos associ-ation with nongrowing tissues For example one DRM1ARPhomologue AP1 was first discovered in cortical tissue fromripe apple fruit [20] In addition Reddy and Poovaiah [19]showed a positive correlation between strawberry (Fragariaananassa) fruit growth and repression of a homologue iden-tified from a library of fruit starved for auxin 120582SAR5 whilebeing highly expressed in mature fruit which have stoppedgrowing More recently Pyrus pyrifolia ARP1 (PpARP1) andPpARP2 expression was detected in the mesocarp tissue ofPear (Pyrus pyrifolia) fruit [24]

Similar data has been seen in kiwifruit with AdDRM1levels reaching a peak in ripe mature fruit (unpublished MWood) and in tomatowhere high levels of the gene transcriptwere localised to the ovaries with a decrease exhibited afterfruit set [26] It is hypothesised that unpollinated ovaries arein a temporally dormant state supported by expression ofcell cycle genes induced after fruit set [26] As these tissuesmay have included seeds and in silico expression profiles showseeds have high levels of SlDRM1 expression further analysisis required in these species to clarify whether this increase inexpression is a result of increases in the maturing fruit fleshor rather in the associated maturing seeds

Increased DRM1ARP gene expression has also beendescribed in tobacco flowers [22] mature stems leaves androots of pea [5] dehisced pollen of tobacco [22] and rootnodules of E umbellata [18] While not at particular high lev-els DRM1ARP transcript has also been detected in petiolesseeds various floral organs and across trunk wood of maturetrees [5 20 22 25 38]

A classical example of tissue aging and transitioning intogrowth suppression is provided in the leaf senescence processArabidopsis max2mutants already described earlier for theirhyperbranching phenotype also exhibit increased longevityduring leaf senescence [39] In ArabidopsisMAX2 transcriptexpression peaks during the early stages of senescence whileAtDRM1 expression continually increases throughout senes-cence reaching a maximumwhen yellowing begins at whichpoint expression remained reasonably constant [40] Thesedata suggest that DRM1ARP is involved in leaf senescencebut later in the process than MAX2 raising the question isMAX2 controlling DRM1ARP

An interesting hypothesis given by Park and Han [25] isfor a putative in planta role for DRM1ARP family membersin repression of cell elongation The authors introduced aninverse correlation between expression of the DRM1ARPhomologue in black locust RpARP (Robinia pseudoacaciaauxin-repressed protein) and the elongation zone of 7-day-old hypocotyls Possible contradictory evidence is found inthe hyperelongated phyb mutant which has increased DRM1transcript expression in Arabidopsis axillary buds [10] Toclarify this AtDRM1 transcript expression would need to bemeasured in the hyperelongating hypocotyl tissue of the phybmutant

PsAD2 another gene identified as being associated withperiods of dormancy showed similar expression profilesoutside of purely dormantmeristematic tissues (accumulated

in axillary buds roots mature leaflets and elongated stems)[41]

5 DRM1ARP and Seed Dormancy

While characteristics of seed dormancy are not generallylinkedwith bud dormancy some striking similarities do existSeed dormancy is defined as the failure of a seed to germinatedespite favourable conditions [42 43] Some chilling isoften required for either seed germination or bud break inperennial species at least However dormancy requires long-term exposure to low temperatures while stratification ofseeds is relatively short term [44]Microarray expression datashow that in Arabidopsis high levels of AtDRM1 transcriptsignificantly reduce with imbibition [45] while transgenicArabidopsis lines overexpressing BrDRM1 or BrARP1 exhib-ited delayed germination phenotypes providing evidencethat DRM1ARP family members might be involved in seeddormancy maintenance Assessment of relative DRM1ARPlevels in a seed germinationmicroarray of barley showed thatDRM1 was unaffected [46]

Osmopriming of seeds is a process which initiatesgermination-related processes but does not allow radicleprotrusion due the high osmolarity solutions used limitingwater availability A study completed on Brassica oleraceacomparing the transcriptome of osmoprimed seeds with thatof water germinated seeds identified that DRM1ARP wasexpressed in seeds germinated on water and not the osmo-primed seeds [15] This finding conflicts with the reductionin transcript with imbibition seen in closely related Ara-bidopsis [45] suggesting that DRM1ARPrsquos expression levelsthroughout germination are not integral to the process butmight be indirectly linked This profile in B oleracea wasshared with a number of stress-associated genes includingcyclophilin superoxide dismutase GRP2 and glutathione-S-transferase [15] providing evidence thatDRM1ARPmight beplaying a more general role in stress response in the seed

6 Regulation of DRM1ARP FamilyGene Expression

Regulation of DRM1ARP has been assessed in response toa number of treatments hormonal sugars and abiotic andbiotic across a number of plant species

61 Hormonal Regulation of DRM1ARP As with many plantgenes DRM1ARP is regulated hormonally In particular anumber of often conflicting lines of evidence exist suggestingthat DRM1ARP family members are regulated by auxinhence many family members being named ARPs (auxin-repressed proteins)

In 1990 a clone named 120582SAR5was identified from cDNAlibrary of strawberry (Fragaria ananassa) fruit starved forauxin [19] and was later found to be a homologue of DRM1ARP Strawberry receptacles (the red-fleshed seedachene-coated organ) were used as a model for auxin action as theachenes are a source of auxin which controls the receptaclegrowth in a pollination-dependent manner Receptacles canbe de-achened and then auxin applied exogenously mimick-ing normal fruit development


Within 6 h from the start of auxin treatment 120582SAR5mRNA levels were significantly lower than those of recepta-cles with no auxin suggesting that high levels of auxin mayhave a role in the downregulation of the DRM1ARP geneRepression was not shown with a weak acid control suggest-ing that any regulatory effects were not simply a result ofauxin acid effectThe auxin analogue selected for these exper-iments was the synthetic naphthalene acetic acid (NAA) asopposed to the naturally occurring indole-3-acetic acid (IAA)for example NAA can induce stronger effects than IAA duein part to being metabolised more slowly in the plant [47]therefore any discrepancies observed between NAA and IAAmay be a consequence of the nature of the two compoundsalthough this remains to be determined Furthermore NAAwas applied at 1mM significantly greater than an acceptedbiologically relevant pmol gramminus1 fresh weight concentra-tions as determined in Arabidopsis and tobacco [48] Polli-nated fruit which have an endogenous source of auxin fromthe resulting achenes provide a more biologically relevantassessment of 120582SAR5 mRNA levels in response to auxin Asexpected 120582SAR5mRNA levels are higher at 3 and 5 days afterpollination (with auxin) than the unpollinated equivalents(no auxin) allowing the conclusion to be drawn that120582SAR5 isrepressed during normal development of strawberry fruit inresponse to exogenous auxin It is noteworthy that the processof de-achening which was integral to this approach wouldlikely have induced a number of stress response pathways notspecific to the exogenously applied auxin which may havehad separate effects on DRM1ARP transcription

A further auxin-repressed homologue from black locustRpARP was identified from an EST database of trunk woodfrom 10-year-old tree with gene expression seen across allsections of the trunk wood [25] RpARP levels decrease uponapplication of exogenous auxin in concentrations as low as01 120583M Upon removal of the source of auxin RpARP levelsincreased again showing a negative relationship betweenDRM1ARP family member expression and auxin treatmentUnfortunately this study also used the synthetic auxin isomerNAAandmost of the experiments were completedwith 1mMauxin beyond the accepted biologically relevant concentra-tion

Analysis of the roles of noncoding sequences showedthat regulatory sequences for auxin repression were locatedin the UTR sequence as opposed to the promoter sequencefor RpARP in transgenic Arabidopsis plants supporting apossible posttranscriptional regulatory mechanism [25]Thisregulation however is not mediated by the characterisedmRNA instability sequences including cis-elements such asthe small auxin upregulated transcript (SAUR) sequencesfound in the 31015840 UTR of several plant genes [49] or themammalian AU-rich elements (AREs) [25 50] The datasuggest a novel regulation mechanism that warrants furthervalidation

While RpARP and indeed 120582SAR5 are showing someevidence for downregulation in their transcript levels inresponse to auxin the timeframe in which this happens canprovide insight into whether or not they are likely to beresponding directly or indirectly to auxin Gene expression

of primary auxin response genes occurs within a matter ofminutes [51ndash54]Those geneswhose regulation by auxin takeslonger than this are generally referred to as secondary auxinresponders and are likely to be further downstream in thesignalling cascade

In contrast analysis carried out in E umbellata showedthat transcript levels in field-grown leaves of a clone iden-tified from a root nodule cDNA library EuNOD-ARP1were induced by exogenous auxin treatment after 6 h [18]Furthermore pear mesocarp discs exhibited an increasein transcript expression of PpARP1 and PpARP2 with IAAtreatment [24] These pieces of data contradict previousfindings in strawberry [19] black locust [25] and in pea [23]The type and age of the tissue assessed are a major differencebetween these studies which might explain these variationsin auxin response

A further conflicting finding has been described inArabidopsis where auxin overproducing 35SYUCCA Ara-bidopsis lines displayed no change in AtDRM1 expressioncompared to wild-type plants (Table 2) [13] These mutantsshowed a reduced branching phenotype and approximatelytwice the amount of free auxin compared with WT plants[55] As such Finlayson [13] argued that DRM1ARP isunlikely to be affected directly by auxin if at all

More recently transgenic Arabidopsis lines overexpress-ing the coding region of BrDRM1 and BrARP1 which exhibitreduced hypocotyl growth in dark-grown seedlings showeda compounded growth suppression with NAA application[16] That these constructs used the coding region only andtherefore do not contain any UTR sequence which wouldbe required for an auxin response based on the Robiniapseudoacacia data [25] suggests that any auxin responses inthis gene family might be regulated by different mechanismsin different species

Overall these data question whether or not DRM1ARPfamily members are regulated by auxin with conflicting dataemerging from various experimental setups Thorough anal-yses of auxin regulation in planta with a focus on biologicalrelevance are therefore required

Only scarce data are available pertaining to the effectsof hormones other than auxin on expression of DRM1ARPfamily members In pea it was shown that PsDRM1 is inducedwhen samples were treated with ABA [23] while GA hadno effect on transcript levels Despite being the sole piece ofpublished data onABAregulation ofDRM1ARP the gene hasbeen used as a genetic marker for ABA response in studiesof fruit set in tomato [26] Vriezen et al [26] argue that thedecrease in DRM1ARP after fruit set might be due to lowerlevels of ABA in the ovary after induction of fruit growthalthough this remains to be assessed further

Few data are available on any response of DRM1ARPfamily members to cytokinin treatment however it wouldbe expected that cytokinin treatment which is generallyassociated with an increase in cell division would lead toa decrease in transcript levels of DRM1ARP The only dataavailable are from a transcriptomic approach comparingAra-bidopsis seedlings treated with BAPwith nontreated plants Adecrease in both AtDRM1 and AtDRM2 levels was observed


but further validation of this finding remains to be completed[56]

62 Regulation of DRM1ARP Family Members by Sugars Aplant needs carbohydrates in the form of sugars to grow Inparticular sugar is required for expression of the cell cyclegene CyclinD3 [57 58] Similarly carbohydrate metabolismgenes have been shown to change over the three distinctphases of dormancy in the buds of the perennial weed leafyspurge [59] making a clear link between sugar levels andratios to dormancy

An association between sugar and DRM1ARP was firstdescribed in black locust in 2003 [25] In an attempt to furtherunderstand auxin regulation of RpARP sucrose was analysedas a factor associated with auxin-mediated growth Sugardeprivation led to an increase in RpARP gene expression Asdiscussed above in this paperrsquos findings on auxin regulationthe age of this tissue and therefore whether or not it wasgrowing was not mentioned in the text and age of the tissuemay have an impact on the findings Upon discovery ofthe sugar response the upstream promoter sequence wasscreened and four sugar responsive elements (SREs) knownto be responsible for sugar repression of the 120572-amylase genein rice [60] were identified [61] Furthermore it was shownthat the promoter sequencewas required tomediate the sugarresponse [25]

A subsequent in-depth study of sugar regulation ofDRM1ARP amongst other genes was carried out by Gonzaliet al [62] In support of the findings of Park and Han [25]they described almost a complete repression of AtDRM1 bysucrose fructose and glucose but not by other sugars includ-ing turanose and mannitol As modulation of AtDRM1 wasseen as a result of more than one sugar type it was concludedthat AtDRM1 could be a low-specificity sensor of sugars[62]

More recently studies of the reduced branching tin (tillerinhibition) mutant in wheat (Triticum aestivum) have drawna link between sugar levels dormancy status andDRM1ARP[11] The dormant buds of tin show reduced sucrose con-tent transcriptional responses in both sucrose-inducible andsucrose starvation-inducible markers (downregulation andupregulation resp) and reduction in transcript expression ofcell cycle markers leading to the hypothesis that the extensivebud dormancy seen in the mutant is due to cessation of celldivision due to diversion of sucrose away from the budsThe dormancy status of the buds of tin plants was confirmedby DRM1ARP and TBL1 transcript expression assessmentleading to an additional hypothesis that DRM1ARP (as wellas TBL1) are involved in dormancy responses specificallyrelated to sucrose starvation [11] Data from kiwifruit haveshown that sucrose levels accumulate in dormant buds overwinter and reduce again prior to bud break in spring [63]Indeed application of hydrogen cyanamide is associated witha rapid decrease in both detectable sucrose levels [63] andDRM1ARP transcript levels [7]

Work in Arabidopsis showed a somewhat contradictoryresult [6] A microarray was carried out allowing categori-sation of genes categorised as either up- or downregulatedin response to inflorescence decapitation Both AtDRM1

and AtDRM2were downregulated in buds upon decapitation[6] A search for regulatory elements enriched in promotersequences of either group identified Sugar Responsive Ele-ments (SREs) as being highly conserved in genes downreg-ulated with decapitation It must be noted however that thiswork only analysed the initial 500 bp upstream of the startcodon and as such possibly neglected the majority of thepromoter sequences Furthermore these motifs remain to beassessed biologically which will inevitably provide a morerobust basis for any hypotheses These conflicting pieces ofdata suggest that DRM1ARP family members are unlikely tobe directly regulated by sugar levels

63 Regulation of DRM1ARP Family Members by Abioticand Biotic Stresses Across the plant kingdom DRM1ARP isincreasingly being linked to stress responses whether they area result of abiotic or biotic factors

Increases in DRM1ARP transcript levels have been asso-ciated with the light signalling pathway mutant phyb inboth Arabidopsis and Sorghum (Sorghum bicolor) [10 2728] (Table 2) phyb mutants have reduced bud outgrowthwith a concomitant increase in DRM1 expression [10 2728] providing support for the hypothesis that DRM1ARP isinvolved in growth suppression in bud andhypocotyls tissues

Other abiotic stress factors have also been consideredAn increase in DRM1ARP expression with cold treatmentor salt stress has been documented in pea [23] Capsicumannuum [17] and the close relative of Arabidopsis B rapa[16] During times of eco-dormancy due to cold it might beanticipated that DRM1ARP expression is high suggesting arole for DRM1ARP in temperature signalling An interestingset of experiments considered the effect of various growthregulators and abiotic stresses in conjunction with auxinapplication onRpARP gene expression [25] Data showed thatRpARP expression was induced either with or without auxinby cold stress providing evidence for cold stress overridingany auxin response Other treatments showed no significanteffect on transcript profiles These data provide furtherevidence for DRM1ARP family members not being directlyregulated by auxin

DRM1ARP transcript expression has been assessed inresponse to further abiotic factors including drought con-ditions in peanut (Arachis hypogaea) [14] and heat shock inB rapa [16] with both conditions leading to an increase inexpression

AtDRM1 and AtDRM2 levels are increased in the SNF2Brahma-type AtCHR12 chromatin-remodelling gene overex-pression lines introduced earlier which undergo arrest ofaxillary bud outgrowth and a reduction in inflorescence boltgrowth only in response to stress conditions [12] Converselytranscript levels of AtDRM1 and AtDRM2 are downregulatedin Atchr12 knock-out mutants [12] These findings suggestthat AtDRM1ARP genes might be acting downstream ofAtCHR12 in a stress-modulated pathway

As well as being involved in responses to abiotic fac-tors DRM1ARP family members have also been linked tobiotic stress responses A cell death-based assay was under-taken using transient virus-induced gene silencing of DRM3(homologue of a closely related DRM family member


Nucleus

Growth

CytosolReceptor

Mature fruitseed podRestricted cell elongation

LeavesAssociated with leaf maturation

Axillary budsPreventing bud outgrowth

HypocotylsstemsPreventing elongationDRM1

ARP

Mature dry seedsPreventing germination

Responseprotein

PPPP

PP

MKKK MKKKinactive

inactive

inactive

active

active

active

MKK MKK

MKMK

DRM1ARP

RootsAssociated with maturetissueand pathogen response

Abiotic + biotic + endogenous factors

Figure 2 Schematic diagram of hypothetical in planta functions of DRM1ARP Mitogen activated protein (MAP) kinase kinase kinase(MKKK) MAP kinase kinase (MKK) andMAP kinase (MK) are representative of a generalised signalling cascade resulting in expression ofDRM1ARPrsquos in response to a range of abiotic biotic and endogenous factors DRM1ARP proteins are hypothesised to play a role in growthinhibition via a currently unknown pathway

At1g56220) in Nicotiana benthamiana Plants silenced forNbDRM3 and challenged with a number of bacterial effectorswere compromised in their pathogen-associated molecularpattern-triggered immunity (PTI) [21]

These data combined with the fact that DRM1ARP pro-teins in kiwifruit have been shown to be IDPs [7] a classof proteins often associated with stress response pathways inplants as well asmultiple lines of evidence showing transcriptexpression outside of purely dormant tissue provide increas-ing evidence that DRM1ARPs are involved in responding tosuboptimal conditions whether they be abiotic or biotic andwhether this is in meristematic tissue with (by definition) thepotential to go dormant or not

7 DRM1ARP Mutants

Analysis of plant lines either overexpressing a gene and itsresulting protein or downregulating expression is a powerfultool for characterizing a genersquos role in planta

Studies conducted in black locust [25] stated that overex-pression of full length RpARP cDNA either with or withoutthe UTRs resulted in Arabidopsis plants with no changein phenotype compared with wild-type plants Similarlyoverexpression of EuNOD-ARP1 cDNA inArabidopsis had nonoticeable phenotype [18]

More recently data have emerged claiming a numberof alterations to the visible phenotype of Arabidopsis plants


overexpressing cDNA of either of two homologues of DRM1andARP1 from B rapaThese included a reduction in vegeta-tive growth (petiole length) as well as a reduction in seed pro-ductivity (silique length) A general delay in growth with nosignificant impact on bolting times was also reported result-ing in a reduction in the number of leaves associated withthe vegetative-floral phase transition In addition transgenicplants exhibited a reduction in bolt length and a delay in seedgermination Double knockouts to AtDRM1 and AtDRM2exhibited no change in phenotype [16] These findings are ofparticular interest as they conflict with other species assessedthus far providing further evidence of differing roles ofDRM1ARP family members across different plant species

8 Conclusions and Future Directions

As highlighted in this review DRM1ARP transcript expres-sion has generally been associatedwith dormant buds Excep-tions to this association are seen in tbl1brc1 and 35SYUCCAmutants suggesting that DRM1ARP is not playing a specificrole in dormancy maintenance and as such may not be areliable maker for dormancy release in future studies Fur-thermore the detection of transcripts outside ofmeristematictissues by definition the site of dormancy often in nongrow-ing tissue means that the correlation between DRM1ARPand dormant tissues is more likely representative of a linkbetween the nongrowth status of these tissues as opposed todormancy per se (Figure 2)

This plant-specific gene and its resulting low molecularweight protein are highly conserved and it may be negativelyregulated by auxin Ever since the identification of thedormancy-associated gene DRM1ARP in pea more than adecade ago and more recently in other species its mode ofaction has still to be elucidated Future work will require amultifaceted approach in order to draw conclusions on thefunction ofDRM1ARP in planta Due to the conflicting find-ings around DRM1ARPmutants further analysis on a num-ber of species is required to clarify the effect that either over-expression or downregulation ofDRM1ARP genes has on theplant Transcriptome analysis of these various mutants willprovide further information on the function of DRM1ARPFurther physiological and transcriptional studies consideringadditional abiotic and biotic stress factors as well as thosealready described in more depth will be of interest Antibod-ies would be helpful to use for protein localisation studieswhich could complement promoter GUS analysis lookinginto the means of transcriptional regulation of this genefamily Finally protein-protein interaction experiments suchas yeast-2-hybrid assays could allow elucidation of bindingpartners

Through identification of genetic pathways the genes areinvolved in identification of the regulatory mechanisms ofthe genes localisation studies at the protein level and identi-fication of binding partners the function of DRM1ARP willbe clarified

Conflict of Interests

No conflict of interests exists for any of the authors in relationto the work discussed in this paper

Acknowledgments

Thanks are due to Minna Pesonen and David Moore for thedevelopment of graphic images (Figures 1 and 2 resp)

References

[1] G A Lang J D Early G C Martin and R L Darnell ldquoEndo-para- and ecodormancy physiological terminology and classi-fication for dormancy researchrdquo HortScience vol 22 no 3 pp371ndash377 1987

[2] K VThimann and F Skoog ldquoOn the inhibition of bud develop-ment and other functions of growth substances in Vicia fabardquoProceedings of the Royal Society of London vol 114 no 789 pp317ndash339 1934

[3] M A Domagalska and O Leyser ldquoSignal integration in thecontrol of shoot branchingrdquo Nature Reviews Molecular CellBiology vol 12 no 4 pp 211ndash221 2011

[4] Y Seto H Kameoka S Yamaguchi and J Kyozuka ldquoRecentadvances in strigolactone research chemical and biologicalaspectsrdquo Plant and Cell Physiology vol 53 no 11 pp 1843ndash18532012

[5] J P Stafstrom B D Ripley M L Devitt and B DrakeldquoDormancy-associated gene expression in pea axillary budsCloning and expression of PsDRM1 and PsDRM2rdquo Planta vol205 no 4 pp 547ndash552 1998

[6] K Tatematsu S Ward O Leyser Y Kamiya and E NambaraldquoIdentification of cis-elements that regulate gene expressionduring initiation of axillary bud outgrowth in ArabidopsisrdquoPlant Physiology vol 138 no 2 pp 757ndash766 2005

[7] M Wood G M Rae R-M Wu et al ldquoActinidia DRM1mdashan intrinsically disordered protein whose mRNA expression isinversely correlated with spring budbreak in kiwifruitrdquo PLoSONE vol 8 no 3 Article ID e57354 2013

[8] D P Horvath J V Anderson W S Chao and M E FoleyldquoKnowing when to grow signals regulating bud dormancyrdquoTrends in Plant Science vol 8 no 11 pp 534ndash540 2003

[9] XHuang T Xue S Dai S Gai C Zheng andG Zheng ldquoGenesassociated with the release of dormant buds in tree peonies(Paeonia suffruticosa)rdquoActa Physiologiae Plantarum vol 30 no6 pp 797ndash806 2008

[10] S A Finlayson S R Krishnareddy THKebrom and J J CasalldquoPhytochrome regulation of branching in Arabidopsisrdquo PlantPhysiology vol 152 no 4 pp 1914ndash1927 2010

[11] T H Kebrom P M Chandler S M Swain R W King R ARichards andW Spielmeyer ldquoInhibition of tiller bud outgrowthin the tinmutant of wheat is associated with precocious intern-ode developmentrdquo Plant Physiology vol 160 no 1 pp 308ndash3182012

[12] L Mlynarova J-P Nap and T Bisseling ldquoThe SWISNF chro-matin-remodeling gene AtCHR12 mediates temporary growtharrest in Arabidopsis thaliana upon perceiving environmentalstressrdquoThe Plant Journal vol 51 no 5 pp 874ndash885 2007

[13] S A Finlayson ldquoArabidopsis TEOSINTE BRANCHED1-LIKE 1regulates axillary budoutgrowth and is homologous tomonocotTEOSINTE BRANCHED1rdquo Plant and Cell Physiology vol 48no 5 pp 667ndash677 2007

[14] GGovindHVokkaligaThammegowda P JayakerKalaiarasi etal ldquoIdentification and functional validation of a unique set ofdrought induced genes preferentially expressed in response togradual water stress in peanutrdquoMolecular Genetics and Genom-ics vol 281 no 6 pp 591ndash605 2009


[15] Y Soeda M C J M Konings O Vorst et al ldquoGene expressionprograms during Brassica oleracea seedmaturation osmoprim-ing and germination are indicators of progression of the germi-nation process and the stress tolerance levelrdquo Plant Physiologyvol 137 no 1 pp 354ndash368 2005

[16] J Lee C-T Han and Y Hur ldquoMolecular characterization of theBrassica rapa auxin-repressed superfamily genes BrARP1 andBrDRM1rdquoMolecular Biology Reports vol 40 no 1 pp 197ndash2092013

[17] E W Hwang K A Kim S C Park M J Jeong M O Byunand H B Kwon ldquoExpression profiles of hot pepper (Capsicumannuum) genes under cold stress conditionsrdquo Journal of Bio-sciences vol 30 no 5 pp 657ndash667 2005

[18] H B Kim H Lee C J Oh N H Lee and C S An ldquoExpressionof EuNOD-ARP1 encoding auxin-repressed protein homolog isupregulated by auxin and localized to the fixation zone in rootnodules ofElaeagnus umbellatardquoMolecules andCells vol 23 no1 pp 115ndash121 2007

[19] A S N Reddy and B W Poovaiah ldquoMolecular cloning andsequencing of a cDNA for an auxin-repressed mRNA correla-tion between fruit growth and repression of the auxin-regulatedgenerdquo Plant Molecular Biology vol 14 no 2 pp 127ndash136 1990

[20] S A Lee R C Gardner andM Lay-Yee ldquoAn apple gene highlyexpressed in fruitrdquo Plant Physiology vol 103 no 3 p 1017 1993

[21] S Chakravarthy A C Velasquez S K Ekengren A Collmerand G B Martin ldquoIdentification of Nicotiana benthamianagenes involved in pathogen-associated molecular pattern-trig-gered immunityrdquoMolecular Plant-Microbe Interactions vol 23no 6 pp 715ndash726 2010

[22] C Steiner J Bauer N Amrhein and M Bucher ldquoTwo novelgenes are differentially expressed during early germination ofthe male gametophyte of Nicotiana tabacumrdquo Biochimica etBiophysica Acta vol 1625 no 2 pp 123ndash133 2003

[23] J P Stafstrom ldquoRegulation of growth and dormancy in pea axil-lary budsrdquo in Dormancy in Plants J-D Viemont and J CrabbeEds pp 331ndash346 CAB International Wallingford UK 2000

[24] H-Y Shi Y-X Zhang and L Chen ldquoTwo pear auxin-repressed protein genes PpARP1 and PpARP2 are predomi-nantly expressed in fruit and involved in response to salicylicacid signalingrdquo Plant Cell Tissue and Organ Culture pp 1ndash82013

[25] S Park and K Han ldquoAn auxin-repressed gene (RpARP) fromblack locust (Robinia pseudoacacia) is posttranscriptionally reg-ulated and negatively associated with shoot elongationrdquo TreePhysiology vol 23 no 12 pp 815ndash823 2003

[26] W H Vriezen R Feron F Maretto J Keijman and C MarianildquoChanges in tomato ovary transcriptome demonstrate complexhormonal regulation of fruit setrdquo New Phytologist vol 177 no1 pp 60ndash76 2008

[27] T H Kebrom B L Burson and S A Finlayson ldquoPhytochromeB repressesTeosinte Branched1 expression and induces sorghumaxillary bud outgrowth in response to light signalsrdquo PlantPhysiology vol 140 no 3 pp 1109ndash1117 2006

[28] T H Kebrom T P Brutnell and S A Finlayson ldquoSuppressionof sorghum axillary bud outgrowth by shade phyB and defoli-ation signalling pathwaysrdquo Plant Cell and Environment vol 33no 1 pp 48ndash58 2010

[29] A K Dunker J D Lawson C J Brown et al ldquoIntrinsically dis-ordered proteinrdquo Journal of Molecular Graphics and Modellingvol 19 no 1 pp 26ndash59 2001

[30] L M Iakoucheva C J Brown J D Lawson Z Obradovic andA K Dunker ldquoIntrinsic disorder in cell-signaling and cancer-associated proteinsrdquo Journal of Molecular Biology vol 323 no3 pp 573ndash584 2002

[31] Y Minezaki K Homma A R Kinjo and K NishikawaldquoHuman transcription factors contain a high fraction of intrin-sically disordered regions essential for transcriptional regula-tionrdquo Journal of Molecular Biology vol 359 no 4 pp 1137ndash11492006

[32] A Garay-Arroyo J M Colmenero-Flores A Garciarrubio andA A Covarrubias ldquoHighly hydrophilic proteins in prokaryotesand eukaryotes are common during conditions of water deficitrdquoThe Journal of Biological Chemistry vol 275 no 8 pp 5668ndash5674 2000

[33] J M Mouillon P Gustafsson and P Harryson ldquoStructuralinvestigation of disordered stress proteins Comparison of full-length dehydrins with isolated peptides of their conservedsegmentsrdquo Plant Physiology vol 141 no 2 pp 638ndash650 2006

[34] S Chakrabortee C Boschetti L J Walton S Sarkar D CRubinsztein and A Tunnacliffe ldquoHydrophilic protein associ-ated with desiccation tolerance exhibits broad protein stabiliza-tion functionrdquo Proceedings of the National Academy of Sciencesof the United States of America vol 104 no 46 pp 18073ndash180782007

[35] D Kovacs B Agoston and P Tompa ldquoDisordered plantLEA proteins as molecular chaperonesrdquo Plant Signaling andBehavior vol 3 no 9 pp 710ndash713 2008

[36] D Kovacs E Kalmar Z Torok and P Tompa ldquoChaperoneactivity of ERD10 and ERD14 two disordered stress-relatedplant proteinsrdquo Plant Physiology vol 147 no 1 pp 381ndash3902008

[37] J Petersen S K Eriksson P Harryson et al ldquoThe lysine-richmotif of intrinsically disordered stress protein CDeT11-24 fromCraterostigma plantagineum is responsible for phosphatidic acidbinding and protection of enzymes from damaging effectscaused by desiccationrdquo Journal of Experimental Botany vol 63no 13 pp 4919ndash4929 2012

[38] G S Ross M L Knighton and M Lay-Yee ldquoAn ethylene-related cDNA from ripening applesrdquo Plant Molecular Biologyvol 19 no 2 pp 231ndash238 1992

[39] H R Woo K M Chung J H Park et al ldquoORE9 an F-boxprotein that regulates leaf senescence inArabidopsisrdquo Plant Cellvol 13 no 8 pp 1779ndash1790 2001

[40] E Breeze E Harrison S McHattie et al ldquoHigh-resolution tem-poral profiling of transcripts duringArabidopsis leaf senescencereveals a distinct chronology of processes and regulationrdquo PlantCell vol 23 no 3 pp 873ndash894 2011

[41] YMadoka andHMori ldquoTwonovel transcripts expressed in peadormant axillary budsrdquo Plant and Cell Physiology vol 41 no 3pp 274ndash281 2000

[42] J D Bewley ldquoSeed germination and dormancyrdquo Plant Cell vol9 no 7 pp 1055ndash1066 1997

[43] G M Simpson Seed Dormancy in Grasses Cambridge Univer-sity Press Cambridge UK 1990

[44] A Rohde and R P Bhalerao ldquoPlant dormancy in the perennialcontextrdquo Trends in Plant Science vol 12 no 5 pp 217ndash223 2007

[45] M Schmid T S Davison S R Henz et al ldquoA gene expressionmap ofArabidopsis thaliana developmentrdquoNature Genetics vol37 no 5 pp 501ndash506 2005

[46] J M Barrero M J Talbot R G White J V Jacobsenand F Gubler ldquoAnatomical and transcriptomic studies of the


coleorhiza reveal the importance of this tissue in regulatingdormancy in Barleyrdquo Plant Physiology vol 150 no 2 pp 1006ndash1021 2009

[47] EM Beyer and PWMorgan ldquoEffect of ethylene on the uptakedistribution and metabolism of indoleacetic acid-1-14C and -2-14C and naphthaleneacetic acid-1-14Crdquo Plant Physiology vol 46no 1 pp 157ndash162 1970

[48] Y Izumi AOkazawa T Bamba A Kobayashi and E FukusakildquoDevelopment of a method for comprehensive and quantita-tive analysis of plant hormones by highly sensitive nanoflowliquid chromatography-electrospray ionization-ion trap massspectrometryrdquo Analytica Chimica Acta vol 648 no 2 pp 215ndash225 2009

[49] PGil andP J Green ldquoMultiple regions of theArabidopsis SAUR-AC1 gene control transcript abundance the 31015840 untranslatedregion functions as an mRNA instability determinantrdquo TheEMBO Journal vol 15 no 7 pp 1678ndash1686 1996

[50] C Y A Chen and A B Shyu ldquoAU-rich elements charac-terization and importance in mRNA degradationrdquo Trends inBiochemical Sciences vol 20 no 11 pp 465ndash470 1995

[51] S Abel and A Theologis ldquoEarly genes and auxin actionrdquo PlantPhysiology vol 111 no 1 pp 9ndash17 1996

[52] J L Key NM Barnett andC Y Lin ldquoRNA and protein biosyn-thesis and the regulation of cell elongation by auxinrdquo Annals oftheNewYorkAcademy of Sciences vol 144 no 1 pp 49ndash62 1967

[53] A Theologis T V Huynh and R W Davis ldquoRapid inductionof specific mRNAs by auxin in pea epicotyl tissuerdquo Journal ofMolecular Biology vol 183 no 1 pp 53ndash68 1985

[54] A Theologis and P M Ray ldquoEarly auxin-regulated polyadeny-lylated mRNA sequences in pea stem tissuerdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 79 no 2 pp 418ndash421 1982

[55] Y Zhao S K Christensen C Fankhauser et al ldquoA role for flavinmonooxygenase-like enzymes in auxin biosynthesisrdquo Sciencevol 291 no 5502 pp 306ndash309 2001

[56] D L Lindsay Cytokinin-induced gene expression in Arabidopsis[Degree of doctor of philosophy] Department of Biology Univer-sity of Saskatchewan SaskatoonCanada 2006

[57] J M S Healy M Menges J H Doonan and J A H Mur-ray ldquoThe Arabidopsis D-type cyclins CycD2 and CycD3 bothinteract in vivo with the PSTAIRE cyclin-dependent kinaseCdc2a but are differentially controlledrdquoThe Journal of BiologicalChemistry vol 276 no 10 pp 7041ndash7047 2001

[58] E A Oakenfull C Riou-Khamlichi and J A HMurray ldquoPlantD-type cyclins and the control of G1 progressionrdquo PhilosophicalTransactions of the Royal Society B vol 357 no 1422 pp 749ndash760 2002

[59] W S Chao and M D Serpe ldquoChanges in the expression ofcarbohydrate metabolism genes during three phases of buddormancy in leafy spurgerdquo Plant Molecular Biology vol 73 no1-2 pp 227ndash239 2010

[60] C A Lu E K Lim and S M Yu ldquoSugar response sequence inthe promoter of a rice120572-amylase gene serves as a transcriptionalenhancerrdquo The Journal of Biological Chemistry vol 273 no 17pp 10120ndash10131 1998

[61] E Nambara M Okamoto K Tatematsu R Yano M Seo andY Kamiya ldquoAbscisic acid and the control of seed dormancy andgerminationrdquo Seed Science Research vol 20 no 2 pp 55ndash672010

[62] SGonzali E Loreti C Solfanelli GNovi AAlpi andP PerataldquoIdentification of sugar-modulated genes and evidence for in

vivo sugar sensing inArabidopsisrdquo Journal of Plant Research vol119 no 2 pp 115ndash123 2006

[63] A C Richardson E F Walton H L Boldingh and J S Meek-ings ldquoSeasonal carbohydrate changes in dormant kiwifruitbudsrdquo in Proceedings of the 6th International Symposium onKiwifruit vol 753 pp 567ndash572 2007

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



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ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


signal integrator brc1tbl1 have also been studied in orderelucidate alternate pathways involved in this critical processThese studies relied heavily on the use of a genetic marker fordormancy statusmdashdormancy-associated gene 1 (DRM1)auxinrepressed protein (ARP) This review will present literatureassociated with DRM1ARP from a number of species (sum-marised in Table 1) and will discuss the relevance of usingDRM1ARP as a molecular marker for dormant tissues

2 DRM1ARP and Dormancy

The first studied member of the DRM1ARP gene familywhose transcript expression was linked with dormancy phys-iology PsDRM (dormancy-associated gene)-1 was isolatedfromdifferential display performedwith cDNA libraries fromdormant and growing axillary buds of pea To consider therelationship between expression of this gene and axillarybud dormancy Stafstrom et al [5] decapitated Alaska peaplants By removing the apical buds of the pea plants thebud can be released from paradormancy (apical dominance)allowing outgrowth of the axillary buds (Figure 1) PsDRM1expression was analysed by northern blot in the bud atvarious time points after decapitation and revealed that uponrelease of dormancy PsDRM1 levels decreased 20-fold witha concomitant increase in the expression of the cell cyclemarker gene PsRPL27 [5]

Two homologues to PsDRM1 have been identified inArabidopsisAtDRM1 (At1g28330) and AtDRM2 (At2g33830formally known as AtDRM1-homologue) As in pea a decap-itation was conducted in Arabidopsis showing that AtDRM1and AtDRM2 expression levels decreased with the release ofparadormancy [6] Subsequent expression levels increasedfrom 24 h after decapitation due to a putative apical dom-inance from the primary axillary outgrowth leading toparadormancy in the lower buds

Dormancy release experiments performedwithAdDRM1the DRM1ARP homologue in Actinidia deliciosa (kiwifruit)using hydrogen cyanamide (commercially available asHiCane) as a dormancy release agent show the same expres-sion profiles [7] Treatment with hydrogen cyanamide wasused to release the apical buds from endodormancy (com-pared with decapitation initiating release of apical budsfrom paradormancy in pea and Arabidopsis) Upon releaseof bud dormancy the characteristic decrease in AdDRM1expression was seen In the same experiment the expressionof AdCDKB (cyclin-dependant protein kinase B) a markerfor growth from kiwifruit was assessed Cyclin-dependentkinases (CDKs) are known to be involved in the reinitiation ofcell cycle progression through the G

1-S phase transition [8]

As AdDRM1 levels decrease AdCDKB expression increases[7]

Further evidence of an association of DRM1ARP tran-scripts with periods of dormancy is seen in PsARP (Paeo-nia suffruticosa auxin-repressed protein) a gene identifiedas being associated with the release of dormant buds oftree peony PsARP showed a sharp increase prior to bud breakand then dropped to low levels as the buds grew [9]

In most cases increases in DRM1ARP expression areassociated with reduced branching phenotypes phyb [10] tin

Dormant axillary buds Buds released from Axillary bud outgrowthdormancy

SAM

Figure 1The ldquodecapitation experimentrdquo used by Stafstrom et al [5]to induce release of dormancy

[11] andCHR12OX [12] and decreases inDRM1ARP expres-sion are associated with increased branching phenotypesaxr1-12 [13] max2 [13] and chr12 [12] (Table 2) HoweverDRM1ARP has also been used as a marker for dormancy inArabidopsis in studies of Teosinte branched 1-like or branched1 (TBL1 or BRC1) [13] with less dependability Results showedthat a reduction in mRNA expression of DRM1ARP was notrequired for bud outgrowth leading to the conclusion at thetime that DRM1ARP was probably acting upstream of TBL1[13] AlternativelyDRM1ARP could be acting independentlyofTBL1 In the same study therewas no change inDRM1ARPtranscript levels in hyperbranching 35SYUCCA where youmay anticipate a reduction in expression providing furtherevidence that DRM1ARP may not be playing a role specifi-cally in holding back bud outgrowth

These findings weaken the argument for DRM1ARP asa molecular marker for dormancy in axillary buds Alterna-tively these data suggest that DRM1ARP is playing a roleas an integrator only under a subset of specific dormancy-related conditions

3 The DRM1ARP Protein Family

Database searches show that theDRM1ARP family is uniqueto plants with homologues found in both monocotyledonsandDicotyledons [25]Multiple protein sequence alignmentsshow high conservation of the DRM1ARP protein prod-uct with two domains clearly identifiable at the amino-terminus and at the carboxy-terminus [7 25] This highconservation across species and indeedmonocotyledons andDicotyledons suggests a potential importance of the actionof this protein in the normal development and physiologyof plants Moreover the protein product is conserved inits size with all 11 species analysed by Park and Han [25]between 11 and 14 kDa (between 109 and 126 amino acidresidues) GFP fusion constructs of EuNOD-ARP1 (EuNOD-ARP1 Elaeagnus umbellata nodule auxin-repressed proteingene 1) a DRM1ARP homologue in the ornamental shrubE umbellata (Japanese silverberry Autumn-Olive) as wellas GFP fusion constructs of Brassica rapa DRM1 and ARP1suggest that it is cytosol-localised [16 18] However in silico


Table1Summaryof

thec

haracteristicsa

ndpu

tativ

efun

ctionof

know

nDRM

1ARP

family

mem

bers

Species

Protein

identifi

erGenen

ame

Possiblefunctio

nPredicted

proteinleng

th(aa)

Predicted

proteinsiz

e(kD)

PredictedpI

Predicted

extin

ction

coeffi

cient

References

Actin

idiadeliciosa

FG458205

AdeDRM

1ID

Ad

DRM

1Axillary

buddo

rmancy

maintenance

andgrow

threpressio

nin

maturefruit

115

12722

1058

19480

Woo

detal2013

[7]

Arabidopsis

thaliana

NP001154378

AtDRM

1Axillary

buddo

rmancy

maintenance

andleafmaturation

122

13406

1071

19480

Tatematsu

etal

2005

[6]

NP850220

AtDRM

2Axillary

buddo

rmancy

maintenance

108

11500

1032

19480

Arachish

ypogaea

AAZ2

0292

AhDRM

1Droug

htstr

essrespo

nse

121

13459

1019

22460

Govindetal

2009

[14]

Brassicaoleracea

AAL6

74436

BoDRM

1Germinationin

subo

ptim

alcond

ition

s105

11352

1010

19480

Soedae

tal2005

[15]

Brassicarapa

ACQ90305

AAO

32054

BrDRM

1BrARP

1

Preventio

nof

germ

ination

preventio

nof

hypo

cotylelong

ation

temperature

andsaltstr

essrespo

nse

128

108

14035

11651

935

1010

18115

19480

Leee

tal2013

[16]

Capsicu

mannu

umAAR8

38881

CaARP

1Coldandsaltstr

essrespo

nse

Onlypartial

available

Hwangetal

2005

[17]

Elaeagnu

sumbellata

AAC

62104

EuNOD-ARP

1Pathogen

respon

sein

root

nodu

les

120

12985

1026

19480

Kim

etal2007

[18]

Fragariaxananassa

Q05349

Fa120582SA

R5Growth

repressio

nin

maturefruit

111

12416

969

19480

Redd

yandPo

ovaiah

1990

[19]

Malus

xdomestica

AAA71994

MdA

P1Growth

repressio

nin

maturefruit

11913060

1001

19480

Leee

tal1993

[20]

Nicotia

nabenthamiana

GW691612

NbD

RM3

PTIimmun

ity127

13623

1036

16960

Chakravarthy

etal

2010

[21]

Nicotia

natabacum

AAO

21304

NtAR

PL11

Growth

repressio

nin

maturep

ollen

andflo

wers

137

14636

1139

20970

Steinere

tal

2003

[22]

Paeoniasuffrutico

saABW

74471

PsAR

PAxillary

buddo

rmancy

maintenance

126

13725

1039

20970

Huang

etal2008

[9]

Pisum

sativ

umAAB8

4193

PsDRM

1Bu

ddo

rmancy

maintenance

and

grow

threpressio

nin

maturetissues

111

12284

1026

19480

Stafstr

om2000

[23]

Stafstr

ometal1998

[5]


Table1Con

tinued

Species

Protein

identifi

erGenen

ame

Possiblefunctio

nPredicted

proteinleng

th(aa)

Predicted

proteinsiz

e(kD)

PredictedpI

Predicted

extin

ction

coeffi

cient

References

Pyrusp

yrifolia

AGG19165

PpAR

P1Growth

repressio

nin

maturefruit

11612631

1026

19480

Shietal2013

[24]

AGG19166

PpAR

P2139

14273

1058

9970

Robiniapseudoacacia

AAG

33924

RpAR

PElon

gatio

nrepressio

nin

hypo

cotyls

115

12641

1022

19480

Park

andHan

2003

[25]

Solanu

mlyc

opersicum

ABH

07900

SlDRM

1Growth

repressio

nin

ldquodormantrdquo

ovariesp

riortofruitset

123

13442

1011

20970

Vriezenetal

2008

[26]








2010 [10]






























































Nucleus

Growth

CytosolReceptor





ARP


Responseprotein

PPPP

PP

MKKK MKKKinactive

inactive

inactive

active

active

active

MKK MKK

MKMK

DRM1ARP






7 DRM1ARP Mutants












Acknowledgments


References











































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table1Summaryof

thec

haracteristicsa

ndpu

tativ

efun

ctionof

know

nDRM

1ARP

family

mem

bers

Species

Protein

identifi

erGenen

ame

Possiblefunctio

nPredicted

proteinleng

th(aa)

Predicted

proteinsiz

e(kD)

PredictedpI

Predicted

extin

ction

coeffi

cient

References

Actin

idiadeliciosa

FG458205

AdeDRM

1ID

Ad

DRM

1Axillary

buddo

rmancy

maintenance

andgrow

threpressio

nin

maturefruit

115

12722

1058

19480

Woo

detal2013

[7]

Arabidopsis

thaliana

NP001154378

AtDRM

1Axillary

buddo

rmancy

maintenance

andleafmaturation

122

13406

1071

19480

Tatematsu

etal

2005

[6]

NP850220

AtDRM

2Axillary

buddo

rmancy

maintenance

108

11500

1032

19480

Arachish

ypogaea

AAZ2

0292

AhDRM

1Droug

htstr

essrespo

nse

121

13459

1019

22460

Govindetal

2009

[14]

Brassicaoleracea

AAL6

74436

BoDRM

1Germinationin

subo

ptim

alcond

ition

s105

11352

1010

19480

Soedae

tal2005

[15]

Brassicarapa

ACQ90305

AAO

32054

BrDRM

1BrARP

1

Preventio

nof

germ

ination

preventio

nof

hypo

cotylelong

ation

temperature

andsaltstr

essrespo

nse

128

108

14035

11651

935

1010

18115

19480

Leee

tal2013

[16]

Capsicu

mannu

umAAR8

38881

CaARP

1Coldandsaltstr

essrespo

nse

Onlypartial

available

Hwangetal

2005

[17]

Elaeagnu

sumbellata

AAC

62104

EuNOD-ARP

1Pathogen

respon

sein

root

nodu

les

120

12985

1026

19480

Kim

etal2007

[18]

Fragariaxananassa

Q05349

Fa120582SA

R5Growth

repressio

nin

maturefruit

111

12416

969

19480

Redd

yandPo

ovaiah

1990

[19]

Malus

xdomestica

AAA71994

MdA

P1Growth

repressio

nin

maturefruit

11913060

1001

19480

Leee

tal1993

[20]

Nicotia

nabenthamiana

GW691612

NbD

RM3

PTIimmun

ity127

13623

1036

16960

Chakravarthy

etal

2010

[21]

Nicotia

natabacum

AAO

21304

NtAR

PL11

Growth

repressio

nin

maturep

ollen

andflo

wers

137

14636

1139

20970

Steinere

tal

2003

[22]

Paeoniasuffrutico

saABW

74471

PsAR

PAxillary

buddo

rmancy

maintenance

126

13725

1039

20970

Huang

etal2008

[9]

Pisum

sativ

umAAB8

4193

PsDRM

1Bu

ddo

rmancy

maintenance

and

grow

threpressio

nin

maturetissues

111

12284

1026

19480

Stafstr

om2000

[23]

Stafstr

ometal1998

[5]


Table1Con

tinued

Species

Protein

identifi

erGenen

ame

Possiblefunctio

nPredicted

proteinleng

th(aa)

Predicted

proteinsiz

e(kD)

PredictedpI

Predicted

extin

ction

coeffi

cient

References

Pyrusp

yrifolia

AGG19165

PpAR

P1Growth

repressio

nin

maturefruit

11612631

1026

19480

Shietal2013

[24]

AGG19166

PpAR

P2139

14273

1058

9970

Robiniapseudoacacia

AAG

33924

RpAR

PElon

gatio

nrepressio

nin

hypo

cotyls

115

12641

1022

19480

Park

andHan

2003

[25]

Solanu

mlyc

opersicum

ABH

07900

SlDRM

1Growth

repressio

nin

ldquodormantrdquo

ovariesp

riortofruitset

123

13442

1011

20970

Vriezenetal

2008

[26]








2010 [10]






























































Nucleus

Growth

CytosolReceptor





ARP


Responseprotein

PPPP

PP

MKKK MKKKinactive

inactive

inactive

active

active

active

MKK MKK

MKMK

DRM1ARP






7 DRM1ARP Mutants












Acknowledgments


References











































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Table1Con

tinued

Species

Protein

identifi

erGenen

ame

Possiblefunctio

nPredicted

proteinleng

th(aa)

Predicted

proteinsiz

e(kD)

PredictedpI

Predicted

extin

ction

coeffi

cient

References

Pyrusp

yrifolia

AGG19165

PpAR

P1Growth

repressio

nin

maturefruit

11612631

1026

19480

Shietal2013

[24]

AGG19166

PpAR

P2139

14273

1058

9970

Robiniapseudoacacia

AAG

33924

RpAR

PElon

gatio

nrepressio

nin

hypo

cotyls

115

12641

1022

19480

Park

andHan

2003

[25]

Solanu

mlyc

opersicum

ABH

07900

SlDRM

1Growth

repressio

nin

ldquodormantrdquo

ovariesp

riortofruitset

123

13442

1011

20970

Vriezenetal

2008

[26]








2010 [10]






























































Nucleus

Growth

CytosolReceptor





ARP


Responseprotein

PPPP

PP

MKKK MKKKinactive

inactive

inactive

active

active

active

MKK MKK

MKMK

DRM1ARP






7 DRM1ARP Mutants












Acknowledgments


References











































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








2010 [10]






























































Nucleus

Growth

CytosolReceptor





ARP


Responseprotein

PPPP

PP

MKKK MKKKinactive

inactive

inactive

active

active

active

MKK MKK

MKMK

DRM1ARP






7 DRM1ARP Mutants












Acknowledgments


References











































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology











































Nucleus

Growth

CytosolReceptor





ARP


Responseprotein

PPPP

PP

MKKK MKKKinactive

inactive

inactive

active

active

active

MKK MKK

MKMK

DRM1ARP






7 DRM1ARP Mutants












Acknowledgments


References











































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology









Acknowledgments


References











































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology





























































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Review Article The Dormancy Marker DRM1/ARP Associated ...Dormancy but a Broader Role In Planta...

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Transcript of Review Article The Dormancy Marker DRM1/ARP Associated ...Dormancy but a Broader Role In Planta...