tmp6163 TMP

Stewart Postharvest Review 2015, 2:2
www.stewartpostharvest.com
ISSN: 1745-9656
Role of auxin depletion in abscission control

Shimon Meir1* Srivignesh Sundaresan1,2, Joseph Riov2, Ishangi Agarwal3 and Sonia Philosoph-Hadas1
1Department
2The
of Postharvest Science of Fresh Produce, Agricultural Research Organization (ARO), The Volcani Center, Bet-Dagan Israel
Robert H Smith Institute of Plant Sciences and Genetics in Agriculture, The Robert H Smith Faculty of Agriculture, Food and Environment,
The Hebrew University of Jerusalem, Rehovot, Israel
3Genotypic Technology Pvt. Ltd, Bangalore, India
Purpose of review: Abscission is a programmed developmental process initiated by auxin depletion. This review
summarizes the mechanisms leading to auxin depletion in the abscission zone (AZ), evaluates the methods for
estimation of the spatio-temporal auxin levels, demonstrates how auxin depletion occurs during natural, stressinduced, and artificially-induced organ abscission, and presents new evidence for early and late events resulting
from auxin depletion which lead to organ abscission.
Findings: Auxin depletion occurs during natural developmental processes which end in organ abscission (leaf and
flower senescence, fruit ripening, and self-pruning) and stress-induced abscission, and following artificial organ
removal in the tomato model system. Stress-induced auxin depletion is mediated by increased ethylene and reactive oxygen species (ROS) production and carbohydrate starvation. Similar changes in auxin-related genes occurred in both flower AZ (FAZ) and leaf AZ (LAZ) following flower or leaf removal, respectively, suggesting a
similar regulation of the abscission process of these organs. Auxin depletion resulted from decreased indole-3acetic acid (IAA) biosynthesis and transport, as well as from enhanced IAA transport autoinhibition (ATA), conjugation and oxidative IAA catabolism. Functional analyses of several target genes delaying abscission, such as Knotted-Like Homeobox Protein1 (KD1), Tomato Proline Rich Protein (TPRP), Ethylene Responsive Factor52 (ERF52), and Ribonuclease LX (LX), shed light on various events operating in response to auxin depletion in tomato FAZ and/or
LAZ. The information gained allows a better understanding of the abscission process driven by auxin depletion,
and might lead to development of improved methods for abscission control in horticultural crops.
Direction for future research: A better understanding of abscission regulation as it pertains to auxin depletion
will require advanced molecular tools such as microarrays, new generation sequencing (NGS), transcriptomic,
functional, and proteomic analyses of target genes and proteins found to operate in the abscission process.
Keywords: abscission zone; auxin homeostasis; carbohydrates; ethylene; functional analysis of target genes; IAA;
ROS; tomato; transcriptome
Introduction
Abscission is a process in which vegetative and reproductive
organs are detached from the mother plant at a specific layer
in response to developmental, environmental, hormonal, and
molecular cues [1-12*]. It is generally accepted that the basipetal polar flux of auxin from the distal organ towards the abscission zone (AZ) renders it insensitive to ethylene, thereby
delaying or preventing abscission. The reduced auxin flow to
the AZ as a result of decreased biosynthesis in the source tissue (the abscising organ), or inhibition of its polar auxin
transport (PAT) are the main factors that render the AZ competent to respond to abscission signals [13-17**, 18, 19*, 20].
A widely accepted working model of abscission [7, 12*] defines four major stages in the abscission process: 1) differentiation of the AZ in the future site of organ detachment; 2) acquisition of competence of the AZ cells to react to abscission
signals; 3) activation of the abscission process in the AZ and
execution of organ detachment; 4) formation of a protective
layer on the proximal surface of the separation layer.
*Correspondence to: Shimon Meir; Email: shimonm@volcani.agri.gov.il
2015 SPS (UK) Ltd.
It is well established that plant hormones apart from auxin and

ethylene regulate abscission. Abscisic acid, jasmonates, and
cytokinins act as abscission-accelerating signals [6, 8, 12*, 2126], while gibberellins, polyamines, and brassinosteroids act as
abscission inhibiting signals [6, 7, 12*, 27-31], but these effects
will not be covered here. This review focuses on evidence that
auxin depletion in the AZ cells is the main signal leading to
acquisition of their competence to respond to ethylene by
execution of organ abscission. The following issues will be
addressed: 1) regulation of auxin levels in plants: biosynthesis,
metabolism, transport, and signaling processes; 2) auxin depletion during natural and stress-induced abscission; 3) elucidation of the sequence of events leading to organ abscission
following artificial auxin depletion in tomato (Solanum lycopersicum). New data, derived from recent customized tomato AZspecific microarray experiments, show regulated changes in
expression of auxin-related genes in the AZs following removal of their auxin source. These data reveal new auxin-related
genes that were not associated until now with the abscission
process.
doi:10.2212/spr.2015.2.2
Meir et al. / Stewart Postharvest Review 2015, 2:2
Abbreviations
ARF
ATA
Aux/IAA
AUX/LAX
AZ
DAP
DPA
ER
ERF
FAZ
GH3
GUS
IAA
iaaM
ILR
KD1
LAX
LAZ
LX
1-MCP
NAZ
NGS
PAT
PCD
PCR
PG
PILS
PIN
PM
qPCR
REV
ROS
TAPG4
SAUR
TF
TIR1/AFB
TPRP
Trp
Auxin Response Factor

IAA Transport Autoinhibition
Auxin Resistant/Indole-3-Acetic
Acid-Inducible
Auxin Resistant/Like Aux
Abscission Zone
Days After Pollination
Days Post Anthesis
Endoplasmic Reticulum
Ethylene Responsive Factor
Flower AZ
Gretchen Hagen3
-Glucuronidase
Indole-3-Acetic Acid
Tryptophan-2-Monooxygenase
IAA-Leu Resistant
Knotted-Like Homeobox Protein1
Like Aux
Leaf AZ
Ribonuclease LX
1-Methylcyclopropene
Non-AZ
New Generation Sequencing
Polar Auxin Transport
Programmed Cell Death
Polymerase Chain Reaction
Polygalacturonase
PIN-LIKES
Pin-formed
Plasma Membrane
Quantitative PCR
REVOLUTA
Reactive Oxygen Species
Tomato Abscission PG4
Small Auxin Upregulated RNA
Transcription Factor
Transport Inhibitor Response1/Auxin
Signaling F-Box
Tomato Proline Rich Protein
L-Tryptophan
Regulation of auxin levels in plants: biosynthesis,

metabolism, transport, and signaling processes
The processes of auxin biosynthesis, metabolism, transport, and
signaling have been extensively reviewed in recent years [3235**, 36-40, 41*, 42*, 43-46**, 47, 48]. Tryptophan (Trp) is the
main precursor for indole-3-acetic acid (IAA) biosynthesis in
plants. There are several proposed IAA biosynthetic pathways
[37, 42*, 48]. In Arabidopsis, the predominant pathway is the
indole-3-pyruvic acid two-step linear IAA biosynthetic pathway,
which is operated by Trp aminotransferase of Arabidopsis and
flavin monooxygenase enzyme families encoded by the YUCCA gene family. Another two-step biosynthetic pathway that
operates in bacteria and plants is the indole-3-acetamide (IAM)
pathway. In this pathway, Trp is converted to IAM by Trp-2monooxygenase (iaaM), which is subsequently hydrolyzed to
IAA by indole-3-acetamide hydrolase.
The distribution and homeostasis of IAA depend on both metabolism (biosynthesis, conjugation, and catabolism) and cellular transport. IAA conjugates play an important role as inactive
storage forms of IAA [35**, 37]. In its free active form, IAA
comprises only 5-25% of the total amount of IAA, depending
on the tissue and plant species. The major forms of IAA conjugates are low molecular weight esters, such as IAA-glucose,
synthesized by IAA-glucose synthase, and amide forms synthesized by the enzyme Gretchen Hagen3 (GH3). The IAA conjugates can be hydrolyzed to form free IAA by IAA-Leu resistant
(ILR), IAA-Ala resistant, or ILR-like enzymes, whereas indole-3
-acetyl aspartate and indole-3-acetyl glutamate act as precursors
of a non-hydrolytic degradation pathway [37, 42*, 45, 48]. IAA
catabolism has been shown to occur either by an oxidative decarboxylation pathway, leading to modifications of both the
side chain and the indole ring, or by a non-decarboxylative oxidation of the indole moiety. Oxidative degradation of auxin
appears to be developmentally important, mainly during fruit
ripening and plant responses to oxidative stress [37]. Most auxin biosynthetic and metabolic pathways occur in low rates,
ranging between 10 nM/h to 1 M/h, with the exception of
auxin conjugation, which has rates as high as 100 M/h [45].
Molecular and biochemical data discussed later in this review
provide evidence that components of auxin homeostasis are
regulated in the AZ tissues.
From the sites of biosynthesis, IAA is transported to other
parts of the plant by diffusion or through active transport. The
directional PAT system distributes auxin from the sites of biosynthesis to basipetal parts of the plant, and is mediated by
influx and efflux carriers. The active influx of auxin in plant
cells is mediated by the influx carriers, Auxin resistant 1/Like
aux1 (AUX/LAX), while efflux carriers belong to the pinformed (PIN) family of proteins [37, 38, 46**]. The PIN family
includes eight members in Arabidopsis thaliana (AtPIN18), and
ten members in both tomato and potato (SlPIN1-10; StPIN110, respectively) [49]. PINs are divided into long and short
PINs according to the length of the hydrophilic protein domain
[37, 46**, 49]. In contrast to the long PIN proteins, which are
located in the plasma membrane (PM), the short AtPIN5 protein is localized in the endoplasmic reticulum (ER), and it participates in the compartmental localization and homeostasis of
auxin. In recent years, a novel putative auxin transport facilitating family that also regulates intracellular auxin homeostasis in
plants has been identified [41]. Named PIN-LIKES (PILS), this
family includes seven members in A. thaliana [41*, 46**]. The
PILS proteins contribute to auxin-dependent regulation of
plant growth by determining the cellular sensitivity to auxin.
PILS proteins regulate intracellular auxin accumulation in the
ER, and thus auxin availability for nuclear auxin signaling [41*,
46**]. Data presented later in this review provide direct evidence for PIN and PILS signaling in tomato AZ tissues.
Auxin enhances its own efflux by rapid modulation of the
abundance of PIN proteins. The transcription of PIN is under
the direct control of auxin, and PIN proteins are also posttranscriptionally regulated by auxin. The auxin feedback regulation of its transport direction and capacity is closely linked to
the canalization hypothesis proposed by Sachs [50]. The cellular and molecular mechanisms for canalization involve the
auxin resistant/IAA-inducible - Auxin Response Factor (Aux/
IAA-ARF) signaling pathway [51]. A similar phenomenon of
canalization is the high velocity IAA transport from a dominant organ, which inhibits the IAA export out of the dominated organ, thereby causing IAA transport autoinhibition (ATA)
in the 'junction' of auxin transport from the two organs [52].
ATA is involved in apical dominance and abscission of dominated organs [52-55]. Other plant hormones (ethylene, cytokinins, gibberellins), small secretory peptides, and environmental signals (light, gravity, abiotic, and biotic stresses) appear to
modulate auxin intracellular compartmentalization by affecting
PIN expression and sub-cellular PIN trafficking [37, 46**].
Ethylene, cytokinins, jasmonates, and strigolactone modulate
PAT via transcriptional and posttranscriptional
regulatory mechanisms of auxin carrier transcription or trafficking. By regulating PIN1 levels in the PM, strigolactone can
influence the capacity of bud-derived auxin to canalize towards
the stem, and thus modulates bud activity and shoot architecture [54].
Two transcription factors (TFs) were found to regulate auxin
biosynthesis, transport, and signaling: KANADI, which has a
Myb-like domain, and REVOLUTA (REV), a Class III Homeodomain-Leucine Zipper TF [56, 57*, 58-62]. These two TFs
have been shown to play antagonistic roles: KANADI acts as a
transcriptional repressor and negatively regulates PIN1 expression, while REV promotes PIN expression and function. Both
TF genes are expressed in the auxin transport routes through
the procambium, cambium, and phloem, thereby playing an
important role in vascular tissue formation and canalization
[60]. Microarray evidence for regulated REV expression in tomato AZs responding to auxin depletion is described below in
this review.
Auxin regulation of transcription events involves a core pathway consisting of the transport inhibitor response1/Auxin signaling F-box (TIR1/AFB) proteins, the Aux/IAA transcriptional repressors, and the ARF TFs. Perception of auxin stabilizes the co-receptor complex of TIR1/AFB and Aux/IAA
proteins, which trigger the proteasome-dependent degradation
of the Aux/IAA transcriptional regulators. Aux/IAAs regulate
auxin-dependent gene transcription by forming dimers with
ARF proteins. The auxin-dependent release of the ARF TFs
leads to the onset of auxin-mediated transcriptional reprogramming [33, 37, 39, 43, 47, 48]. In Arabidopsis, six TIR1/AFB can
interact with 23 different Aux/IAAs to form numerous coreceptor complexes. Each of the Aux/IAA may interact with
up to 19 ARFs to regulate distinct sets of target genes that control different physiological processes. Genome-wide identification, functional analysis, and expression profiling of the Aux/
IAA gene family in tomato were previously reviewed [40]. Most
of the Aux/IAA genes are rapidly induced by auxin, and the
level of several Aux/IAA transcripts increases within a few
minutes following auxin treatment. Therefore, the expression
of these auxin-induced genes can be used as indicators for auxin activity in various tissues, including AZs [63, 64].
Auxin depletion during natural and

stress-induced abscission
Determination of IAA levels

Direct measurements of endogenous levels of IAA (free and
conjugated), using analytical [65, 66] or immunological [66]
methods were developed. Few publications used this analytical
method to demonstrate IAA depletion in the AZ during the
initiation of the abscission process [67, 68, 69**, 70, 71**, 72].
Most determinations of auxin activity in the AZs were based on
the expression of auxin-induced genes. Initially, few auxininduced genes were cloned from the AZ, and their expression
in the AZ was analyzed by polymerase chain reaction (PCR)
[63, 64]. Later, expression profiles of auxin-induced multi-gene
families in various abscission systems were analyzed using microarray [20, 37, 47, 57**, 67, 77**] [or NGS [78*, 79*]
techniques. In transgenic plants, the synthetic auxin-responsive
promoter element DR5 fused to -glucuronidase (GUS),
DR5::GUS, was used for evaluation of IAA levels in the AZs
[70, 71**, 80, 81**]. The use of DR5::GUS has the advantage of
visual assessment, but has a disadvantage for determining IAA
depletion due to the high stability of the GUS protein as compared to the green fluorescent protein, which dissipates rapidly.
Therefore, the green fluorescent protein was used as a reporter
system for studying the temporal expression profiles of promoters for estimation of IAA depletion [82]. In recent years a
new auxin sensor, DII-VENUS, has been developed. This sensor, which is composed of domain II of the Aux/IAA fused to
the VENUS fluorescent protein, provides high-resolution spatio-temporal information about auxin distribution and response
[83]. Unlike the DR5 response, the DII-VENUS sensor is
closely related to auxin concentrations, and does not depend on
the levels of Aux/IAA and ARF proteins, thereby enabling its
use as a quantitative tool. All of these methods monitor auxin
concentration indirectly, via the expression of auxin-induced
genes. In our opinion they act as in vivo bioassays, which have
some weaknesses. Moreover, measuring auxin activity requires
to consider the effects of inhibitors and repressors in the tissues
and/or in the extracts. Hence, the analytical auxin measurements, based on gas chromatography-mass spectrometry determination [65] are more accurate for the determination of low
levels of IAA, and are therefore preferential for estimation of
auxin depletion in the AZ tissues.
Auxin depletion during natural abscission
Abscission of leaves, flowers, floral parts, and overripe fruits is
the last developmental stage of these organs, and is therefore
regarded as natural abscission. The present review examines
whether auxin depletion in these organs, which serves as auxin
sources to their AZs, precedes the execution of ethylenecontrolled abscission.
IAA depletion during senescence-induced flower abscission

Flower senescence and abscission can be ethylene-dependent or
independent [84, 85]. Since the basic premise of this review is
that auxin depletion in the AZ increases the ethylene sensitivity
of the AZ cells, we will focus on ethylene-dependent abscission
of flower buds, open flowers, and petals. Endogenous IAA
levels usually decrease during flower senescence in most flowers that subsequently abscise [86, 87]. Indeed, the abscission of
unfertilized or male flowers may be ascribed to the low levels of

endogenous IAA, which is produced in the ovary [88]. In Begonia, abscising male flower buds contain only 1% of the IAA present in non-abscising female flowers, and the seasonal variation
in male bud abscission coincided with reduction of the IAA
content in the buds [89]. In Lilium, IAA levels decreased in the
gynoecium and petals when the petals started to wilt and senesce, prior to their abscission [90]. IAA level and the expression of 50 auxin-related genes were analyzed in the outer tepals
of two Lilium cultivars that differ in their abscission timing.
Although both cultivars have fully formed AZs, Lilium longiflorum flowers wilted substantially during senescence prior to their
late abscission, while those of the closely related Lilium longiflorum Asiatic hybrid (L.A.) abscised early without wilting [91**].
A clear correlation between auxin levels and abscission timing
of both cultivars was found in relation to senescence markers.
Thus, in L. longiflorum, both free and conjugated-IAA significantly increased as senescence progressed, while free IAA levels
in Lilium L.A. remained low at all developmental stages from
closed bud to abscission, and the portion of IAA-amide conjugate gradually increased. Consistent with the view that declining
IAA levels precede abscission, the ARF7/19-like gene was upregulated in the delayed-abscising genotype, while in the earlyabscising genotype it was down-regulated [91**].
In Dendrobium cut flowers, the floral buds at the top of the inflorescence stalk exhibit early yellowing and abscise. Application of an auxin transport inhibitor or an auxin action inhibitor
to the stigma of open flowers induced high flower abscission
rates [92]. Removal of the open flowers at the distal end of the
pedicel reduced the time to abscission of the remaining pedicel.
IAA placed on the cut surface of the pedicel, counteracted the
effect of flower removal. Application of different auxins delayed senescence and inhibited the abscission of open Dendrobium flowers [92, 93]. These results support the view that auxin is
an endogenous regulator of abscission of Dendrobium floral buds
and flowers. Several other reports show that exogenously applied auxins prevented or delayed abscission of flowers and
floral parts, styles, and stamens [88]. Accordingly, auxin is applied to extend the vase life of several cut flowers, such as
Geraldton wax flowers, Cestrum, and poinsettia [63, 88, 94, 95].
Genetic experiments with Arabidopsis mutants further demonstrated the role of auxin in petal abscission. Mutation in ARF2
[96] and ARF1 and ARF2 [97] delayed senescence and abscission of Arabidopsis petals. Flowers taken from mutants in
which individual family members of the auxin influx carriers
AUX1 and Like-AUX3 (LAX3) were down-regulated, exhibited early abscission. Manipulation of IAA levels in the AZ cells
by activation of the bacterial IAA biosynthetic genes, IAA-Lyssynthetase and iaaM, enhanced or delayed petal abscission, respectively [81**]. It was shown that IAA-Lys-synthetase reduced IAA levels in the cells by conjugating free IAA to IAALysine, while iaaM promoted IAA levels by converting Trp to
indole acetamide.
IAA depletion during senescence-induced leaf abscission

Endogenous IAA decreases at the onset and during senescence
of leaves, and auxin treatment can delay leaf senescence in
some plants [98-100]. Most of the research on leaf senescence
was done by using detached leaves in model systems which do
not show abscission phenotypes (Arabidopsis or flag leaf in
monocots). Therefore, the changes in IAA levels during abscis-
sion were not studied. Only one early report showed a positive
correlation between the decrease in IAA content during senescence of Coleus leaves and their abscission [101]. Moreover, in
monocots and some annual dicots there is no AZ at the base of
the leaf, and the leaves senesce, wilt, and remain dry on the
plant, a process termed marcescence. Therefore, the changes in
IAA content during leaf senescence in these plants, including
the Arabidopsis model system, are less relevant.
IAA depletion during ripening-induced fruit abscission

Fruits typically abscise at the overripe stage of development. In
general, IAA levels decrease in fruit during ripening, and this
decrease coincides with maturation of the seeds, in which most
of the IAA is produced [80, 102-105]. The decrease in IAA
levels starts in tomato fruit as the fruit reaches the breaker stage
[80, 103-104]. The reduction of free IAA levels during ripening
results from the decrease of auxin signal around the seeds [80,
102] and expression of the auxin transport gene families LAX
and PIN with advanced ripening [80], as well as from increased
conjugation of free IAA to its amide conjugates, as GH3 expression is sharply increased with ripening [103-104]. A similar
decrease in IAA levels and an increase in GH3 expression and
indole-3-acetyl-aspartate levels were also observed in grape
berries after reaching the mature green stage [105, 106]. It is
likely, therefore, that auxin depletion in fruit contributes to
subsequent abscission competence. Unfortunately, most studies
of auxin metabolism in ripening fruit were terminated at the
ripe stage, without evaluating fruit at the overripe stage in
which most actual abscission events occur. Only one exception
was reported, in which IAA levels were monitored in oil palm
fruit until abscission. Thus, in developing fruit, the content of
IAA peaked between 60 and 100 days after pollination (DAP),
and subsequently decreased to very low levels between 100 and
120 DAP just before abscission, which occurred 140 DAP
[107**]. Auxin application delayed oil palm fruit abscission
[108]. However, IAA depletion in fruit may be speciesdependent, as in peach several reports demonstrated increased
IAA level during fruit ripening, which is required for fruit softening [109-111].
There has been little work in which fruit ripening was correlated with events occurring in nearby AZs. Recently, two transcriptomic reports demonstrated changes in auxin-related gene
expression in the AZs of mature olive and melon fruit [78*,
79*]. In olive, gene expression was studied 154 days post anthesis (DPA), when fruit started to ripen, and 217 DPA, when fruit
abscised. Numerous auxin-related genes were down-regulated
in the AZ 217 DPA, including auxin biosynthesis genes, ILR1,
auxin transporters LAX1, LAX2 and PIN, TIR1, two AUX/
IAA family members, three ARF family members, and several
auxin-induced genes [78*]. In melon, gene expression was studied at three time points: 36, 38, and 40 DPA. The ethylene climacteric peak and abscission occurred 37 and 40 DPA, respectively. Between 36 to 38 DPA two genes encoding for auxin
effux carriers, four AUX/IAA genes, and one ARF gene were
down-regulated in the AZ [79*]. Between 38 to 40 DPA, 13
other auxin-related genes were down-regulated. These reports
provide the first direct evidence for auxin depletion in the AZ
during mature fruit abscission.
Taken together, the reported data show that the processes of
flower and leaf senescence and fruit ripening generally lead to
Table 1: Examples of auxin depletion mechanisms operated in various stress-induced abscission systems.
Stress type
Plant and abscission system
Mechanisms for auxin depletion
Reference
Domination
Apple fruitlets in clusters
Decrease in PAT; decrease in ATA
13, 16, 17, 143, 157
Grapevine berries in clusters
19*
Cowpea flowers and fruitlets
14
Carbohydrate starvation
(phloem-girdling)
Litchi fruitlets
Decrease in PAT
142
High temperatures
Bell pepper flowers and fruitlets
Decrease in IAA level , decrease in PAT
130
Mango fruitlets
Decrease in PAT
141
Chilling temperatures
Ixora leaves
67
Chilling + high light
Ixora leaves
Increase in IAA oxidation

Decrease in IAA level
Decrease in PAT
Increase in IAA oxidation
Water stress
Cotton leaves
Decrease in PAT
158, 159
Cotton buds, flowers, and fruits

Increase in IAA conjugates level
160, 161
Citrus leaves
Decrease in expression of IAA signaling genes
162
Poplar leaves
Decreased expression of IAA signaling genes
163
Balsam fir needles
164
reduction of endogenous auxin levels, which in turn result in

organ abscission. Sometimes a direct evidence for auxin depletion prior to organ abscission is lacking in these systems, as the
experiments did not analyze IAA levels in the senesced organ
or overripe fruit, but the general pattern was validated in various systems.
IAA depletion during self-pruning of spring shoots in

sweet orange (Citrus sinensis)
Citrus shoot tips abscise at an anatomically distinct AZ that
separates the top part of the shoots into basal and apical portions. This natural process, termed self-pruning, plays an important role in citrus floral bud initiation. Citrus microarray was
used to monitor the expression of genes at several time points:
5 or 3 days before self-pruning, when the shoot tips started to
fall, and at the beginning of self-pruning of spring shoots, when
the AZ was activated [20]. Twenty four auxin-related genes
were differentially altered during these stages of self-pruning;
genes encoding auxin-induced proteins were up-regulated,
while genes encoding ARFs were down-regulated. The authors
concluded that auxin depletion in the AZ of the spring shoots
causes the AZ to become sensitive to ethylene and abscisic
acid, which accelerate the abscission process of the shoot tips
[20].
Ethylene as a mediator of IAA depletion

Ethylene is the main regulator of leaf and flower senescence
and fruit ripening, and is proposed here as a modulator of auxin
depletion in these processes. Unlike the synergistic interactions
between ethylene and auxin controlling specific growth and
developmental processes [112, 113, 114**, 115, 116], the control of both natural and stress-induced abscission (see below)
involves antagonistic effects of ethylene and auxin. Several
68
modes of action were suggested for this negative interaction.

One of the regulatory effects of ethylene on auxin levels, operated through inhibition of auxin transport to the AZs, was
demonstrated long ago [117-122]. Additionally, in various natural abscission systems, ethylene was reported to reduce auxin
levels by increasing the rate of auxin conjugation [120-122].
Auxin depletion during stress-induced abscission

Abscission of different organs is a common response to various
biotic, abiotic, and physiological stresses [2, 4, 6, 119, 123**].
Stress-induced abscission initiated by auxin depletion is mediated by three main intermediate modulators: ethylene, ROS, and
carbohydrate starvation [119, 123**, 124**, 125]. Ethylene production increases in tissues subjected to many stresses, subsequently regulating their auxin levels [126-128]. Stress-induced
ethylene may promote auxin depletion in various abscissing
systems via inhibition of auxin transport to the AZs [117-122,
129, 130].
ROS
ROS can induce organ abscission [131-133] and application of
antioxidants and ROS scavengers can inhibit abscission [67, 68,
134-137]. Several publications reviewed the interplay between
ROS and auxin [124**, 138-140**]. ROS induced by stress conditions have an impact on auxin signaling by affecting auxin
homeostasis at the levels of auxin biosynthesis, metabolism, and
distribution. ROS stimulated auxin catabolism by increasing
decarboxylative and non-decarboxylative oxidation of IAA, IAA
conjugation (ester and amid forms), and GH3 expression, and
inhibited IAA transport by decreasing PIN expression [67, 68,
124**, 138, 139**, 140**]. ROS scavenging genes were induced
by ethylene during abscission of citrus leaves, suggesting that
ethylene induces ROS in this system [138].
Carbohydrate starvation
Numerous stressors, like water stress, high and low light, high
or chilling temperatures, and high sink organ domination, result
in carbohydrate starvation. Abscission of premature fruit,
leaves, flowers, and flower buds is related to low sugar content
[13, 15-17, 141-146]. Auxin application can inhibit some stressinduced organ abscission [15, 146-148], suggesting that the
shortage of carbohydrate is correlated with auxin depletion. In
non-abscissing systems, sugars have also been shown to play
pivotal roles as signaling molecules [149-155156**]. Thus, soluble sugars were reported to increase IAA biosynthesis, free IAA
levels, and IAA transport in these systems [154-155], as well as
to up-regulate early auxin biosynthesis and PIN1 genes, to promote PIN1 abundance in the PM and to down-regulate two
genes of PAT inhibitors [156**]. We anticipate that sugar signaling may ultimately be found to accompany stress-induced
decrease in carbohydrates that result in auxin depletion in
source organs and their AZs. The mechanisms of auxin depletion in various stress-induced abscission systems are summarized in Table 1. Auxin depletion is expected to increase AZ
sensitivity to stress-induced ethylene, thereby resulting in abscission.
Elucidation of the sequence of events leading to organ
abscission following artificial auxin depletion in tomato
Tomato has been extensively used to study flower and fruit
abscission processes. Tomato is a very convenient model system, since tomato plants develop a distinct AZ in the midpoint
of the flower pedicel, referred to as a pedicel AZ or FAZ in
different publications. The anatomy and development of the
tomato FAZ is well established [165-167], as are the proteins
involved in the regulation of the FAZ differentiation and development [168-173]. Since the eighties of the previous century, in
-depth studies have defined enzymes involved in cell separation
in various species. The AZ-specific polygalacturonases (PGs)
and cellulases are particularly well characterized [174-184]. The
AZ cells are defined as specialized cell types that differ from
their adjacent cells in perception and response to ethylene and
auxin [2, 4, 185-187]. Therefore, it is expected that specific TFs
and genes will be specifically expressed in the AZ and not in
the adjacent non-AZ (NAZ) cells. Indeed, in the first transcriptome microarray analysis of the tomato FAZ performed following auxin depletion, several genes were found to be specifically
expressed in the FAZ and not in the basal portion (proximal) of
the pedicel NAZ region [74**]. These genes include several
TFs, such as TOMATO KNOTTED4, Homeobox-Leu zipper13,
TOMATO AGAMOUSE-LIKE2,12, TOMATO PROLINE
RICH PROTEIN (TPRP-F1), KNOTTED1-LIKE HOMEOBOX PROTEIN1 (KD1), Phantastica, and Ovate [74**]. In two
transcriptome analyses comparing gene expression in the tomato FAZ versus the NAZ, including the basal portion (proximal)
and apical portion (distal) pedicel regions, 89 and 1,255 genes,
respectively, were found to be specifically expressed at anthesis
in the FAZ cells, including genes encoding for TFs, hormonerelated proteins, cell wall modification enzymes, lipid metabolism, and others [76**, 77]. Most interestingly, the AZ-specific
gene set include TF genes that encode key regulators of meristem-associated functions, which may be regulated by a signaling pathway that requires auxin supplied from the flower before
the onset of abscission. Suppression of one of the tomato
shoot meristem-associated TF genes, tomato ETHYLENE-
RESPONSIVE FACTOR52 (SIERF52) by RNAi, did not affect FAZ development, but significantly delayed pedicel abscission. This suggests that SlERF52 plays a pivotal role in transcriptional regulation in the FAZ [188**].
In an attempt to perform a functional analysis of 45 AZspecific genes whose expression changed early in the tomato
FAZ following auxin depletion, experiments based on virusinduced gene silencing in the FAZ and LAZ were conducted.
Silencing nine of these 45 genes led to a significant retardation
of pedicel and/or petiole abscission following abscission induction. The role of these nine genes was further examined by
silencing each of them in plants stably transformed with antisense or RNAi constructs driven by an AZ-specific promoter,
Tomato Abscission PG4 (TAPG4). The results showed that
TAPG4::antisense constructs of KD1 [71**] and of TPRP-F1
[189] strongly inhibited both pedicel and petiole abscission.
Conversely, up-regulation of KD1 showed accelerated pedicel
and petiole abscission [71**]. Complementary DNA microarray
and quantitative PCR (qPCR) analyses indicated that regulation
of abscission by KD1 was associated with a change in the abundance of genes related to auxin transporters and signaling components. Measurement of IAA content using the DR5::GUS
auxin reporter assay, confirmed by analytical auxin determination, showed that change, s in KD1 expression modulated the
auxin concentration and response gradient in the FAZ [71**].
In a transcriptomic analysis comparing gene expression in the
tomato FAZ and NAZ in the proximal and distal flanking pedicel regions at anthesis [76**], a region-specific expression of
auxin-related genes was found: 1) METHYLESTERASE1,
which converts IAA methyl ester to IAA, DWARF IN
LIGHT1, which encodes an IAA-amido synthetase, and GH3.6
showed higher transcript levels in the FAZ than in the NAZ; 2)
ARF9 was expressed at higher levels in the proximal (basal) than
in the distal (apical) NAZ region; 3) GH3.1 and a Hookless1
homolog were expressed at higher levels in the distal than in the
proximal NAZ region. This region-specific differential expression of genes involved in the determination of auxin levels suggests that a gradient of auxin concentration formed along the
pedicel regions may be a key factor in regulating the timing of
pedicel abscission [76**]. Indeed, by using the DR5::GUS reporter, such a gradient of IAA concentration was recently found
in VF36 tomato plants, in which the FAZ was also divided into
distal and proximal regions [71**]. Consistent with the initial
location of the auxin-producing source tissue, this gradient occurred according to the following sequence: distal side of NAZ
> distal side of FAZ > proximal side of FAZ > proximal side of
NAZ [71**].
In order to elucidate the molecular changes occurring in the
tomato artificial auxin depletion model system during acquisition of abscission competence in the FAZ following auxin depletion and during execution of pedicel abscission, our group
performed a microarray analysis, using the Affymetrix 10K
oligonucleotide Tomato GeneChip [74**]. In this system, the
flower that serves as an auxin source is removed. Applying IAA
after flower removal or inhibiting ethylene action using 1methylcyclopropene (1-MCP) prior to flower removal inhibited
pedicel abscission, suggesting that pedicel abscission results
from auxin depletion and is ethylene-dependent [74**]. Based
Figure 1: Effect of leaf deblading and ethylene treatment (A) and flower
removal (B) on the kinetics of petiole and pedicel abscission, respectively, in tomato explants. The debladed-leaf explants held in vials with
water were prepared as previously described for the flower explants [72],
and exposed to ethylene (10 ppm for 24 h). The percentage of accumulated pedicel or petiole abscission was monitored at various time intervals following organ removal. The results are means of four replicates
(n=30 explants) SE.
and data showing that different abscission-related processes

occurred asymmetrically between the FAZ proximal and distal
regions were presented [193**]. This asymmetric distribution of
various abscission-related processes might be related to the
auxin gradient demonstrated recently in the tomato FAZ [71**].
Leaf deblading removes the natural source of auxin to an AZ
and promotes abscission [64]. The only report so far describing
the effects of leaf deblading on expression of auxin-related
genes in the LAZ was performed in Mirabilis jalapa [64]. In this
system, transcripts of two auxin-induced genes, Mj-Aux/IAA1
and Mj-Aux/IAA2, were down-regulated as a result of IAA
depletion by leaf deblading or treatment with the IAA transport
inhibitor, 1-naphthylphthalamic acid. Application of IAA to the
cut end of the petioles inhibited their abscission and prevented
the decline in the transcript levels in the LAZ [64].
on the transcriptomic results following the application of the

abscission modulators, an abscission-inducing model was proposed in which the sequence of events occurring during tomato
pedicel abscission was divided into two phases: early events (0
to 4 h after flower removal) and late events (8 to 14 h after
flower removal). The early events probably lead to acquisition
of ethylene sensitivity and abscission competence, while the late
events include processes leading to the execution of pedicel
abscission and development of the defense layer. According to
this model, the decrease in IAA provides the first signal for
abscission. Responses to auxin depletion included downregulation of genes induced by auxin, such as Aux/IAA and
other TF genes, and up-regulation of genes repressed by auxin.
The late events included increased ethylene production, due to
up-regulation of ethylene biosynthesis genes, such as the genes
encoding 1-amino-cyclopropane-1-carboxylate synthase, which
lead in turn to AZ-specific up-regulation of abscission-related
genes. These genes include genes encoding cell wall-modifying
proteins and pathogenesis-related proteins [74**], as well as
genes related to the development of a protective layer on the
surface of the remaining tissue [190]. The late events, which are
ethylene-induced, were inhibited by 1-MCP pretreatment, while
the early events were not affected by the inhibitor. On the other hand, IAA application immediately after flower removal inhibited all the cascade of abscission events and the changes in
the expression of auxin-induced or auxin-repressed genes
[74**]. Two later studies showed a rapid decrease of Aux/IAA
[191] and ARF [70] genes after tomato flower removal. Additionally, quantitative and DR5::GUS data demonstrated a fast
IAA depletion after flower removal [70]. These authors adjusted the proposed abscission model [74**] to the slower abscission rate obtained in their tomato system (0-8 h for the early
events and 16-32 h for the late events), and included the various ARFs in the model [70].
Programmed cell death (PCD) was shown to be another late
event involved in the abscission process. This was based on the
data showing that inhibiting the activity of LX ribonuclease
(LX), an enzyme associated with PCD, delayed tomato leaf
abscission [192]. Indeed, hallmarks of PCD were identified in
the tomato LAZ and FAZ during the late stage of abscission,
To further define auxin-relevant members of tomato LAZ and

FAZ transcriptomes, we recently refined an experimental system based on the abscission responses of debladed tomato
leaves and removed flowers. Deblading of tomato leaves led to
abscission of attached petioles during a period of 8-12 days.
Exposure of the debladed-leaf explants to ethylene treatment
for 24 h accelerated petiole abscission, which was completed
within three days after the ethylene treatment (Figure 1A), at a
similar rate to that of flower pedicel abscission without ethylene
treatment (Figure 1B). RNA collected during petiole and pedicel abscission allowed us to compare transcriptomic changes in
the tomato LAZ and FAZ, respectively, through the use of a
customized AZ-specific microarray chip. The chip included
transcripts identified using NGS of RNA isolated from tomato
AZs at various time points during organ abscission, as well as
transcripts from the Solanaceae genomics network and National Center for Biotechnology Information databases [194]. Here
we present for the first time results from these microarray analyses describing the changes in expression of auxin-related genes
(Figures 2-6). Generally, there is a high similarity in the abscission process of tomato leaves and flowers, with a few exceptions. Most of the auxin-related genes are expressed in both
AZs, but some members of different gene families are expressed specifically in the FAZ or the LAZ.
The results presented in Figure 2 show that most genes encoding auxin influx (LAX family) and auxin efflux (PIN family)
carriers were rapidly down-regulated in both AZs following
IAA depletion, thereby supporting the requirement for auxin
for activation of its transport carriers. The few exceptions were
related to genes that have very low expression levels, such as
LAX4,5 and PIN2,8 in the FAZ and PIN3 in the LAZ. The
down-regulation of PIN5 and PILS family members in the two
AZs, provides the first indication that the regulation of intracellular auxin accumulation in the ER, expected to control auxin
availability for auxin signaling in the nuclei of AZ cells, may be
important for abscission regulation at the cellular level. Two
PILS were up-regulated in the FAZ and one in the LAZ following flower removal or leaf deblading, respectively (Figure 2),
further supporting the role of this novel auxin carrier family in
regulating auxin homeostasis [41]. The REV TF was quickly
down-regulated in the FAZ and LAZ after abscission induction, suggesting that there is a regulatory mechanism for decreasing PIN expression and function in both AZs as a result of
Figure 2: Microarray expression profiles of tomato auxin transport-related genes in the FAZ and LAZ at various time points following abscission induction. The assay included family members of the auxin influx carriers (AUX/LAX), auxin efflux carriers (PINs, PILS) genes, and an auxin-related TF
gene (REV). Samples were taken from the FAZ at 0, 2, 4, 8, and 14 h after flower removal, and from the LAZ at 0, 24, 48, 72, and 96 h after leaf deblading
and ethylene treatment as detailed in the legend of Figure 1. Gene expression levels are indicated with the colored code bars ranging from 0% (light blue)
to 100% (dark blue). Expression levels are based on the percentage of change of the average intensity values of the replicated samples for each time
point. The numbers indicated in the first box of each sample represent average intensities values for all replicates at 0 h. Corresponding Solanum lycopersicum (Solyc) ID and gene names are presented in the left and right sides, respectively.
Figure 3: Microarray expression profiles of tomato IAA-related genes associated with IAA conjugation in the FAZ and LAZ at various time points following abscission induction. The assay included members of the GH3 and ILRs gene families. All other details are as described in the legend of Figure 2.
Figure 4: Microarray expression profiles of tomato auxin-signaling genes in the FAZ and LAZ at various time points following abscission induction. The
assay included members of the Aux/IAA gene family. All other details are as described in the legend of Figure 2.
assay included members of the ARF gene family. All other details are as described in the legend of Figure 2.
assay included members of the SAUR gene family. All other details are as described in the legend of Figure 2.
auxin depletion. Interestingly, it was recently reported that over

-expression of tomato SlREV TF caused the transgenic plants
to produce ectopic flowers from the pedicel AZ [195].
h. These results are in agreement with previous reports regarding the timing of changes in the expression of IAA-responsive
genes in the FAZ following flower removal [74**, 191].
The highly expressed GH3 genes significantly decreased after

leaf deblading (Figure 3), further confirming that GH3 is an
auxin-induced gene [33, 35**, 37]. On the other hand, most
GH3 genes in the FAZ were up-regulated, confirming that increased IAA conjugation is involved in the process of auxin
depletion [104, 105]. To the best of our knowledge, there are
no reports regarding changes in GH3 gene expression in the
AZs after auxin depletion. In contrast to our earlier report describing up-regulation of ILR genes in the FAZ and the proximal NAZ [74**], in the current experiment the ILR genes were
down-regulated in both the FAZ and LAZ after removing the
auxin sources (Figure 3). Further investigation is required to
understand the significance of these changes.
Six ARF genes were exclusively expressed in the FAZ and

three in the LAZ, and all ARF genes were down-regulated after
IAA depletion in both the FAZ and LAZ (Figure 5). These
results cannot be compared to previously reported results for
ARF genes in the tomato FAZ [70], because in the previous
system ethylene was applied after explant preparation. Out of
38 Small Auxin Upregulated RNA (SAUR) genes, 19 genes were
exclusively expressed in the FAZ and four in the LAZ, and a
high variability in the changes of the expression pattern of
SAUR genes was found (Figure 6). There are no previous reports on the expression of SAUR genes in the AZ.
All the Aux/IAA genes that were expressed in the FAZ were
also expressed in the LAZ (Figure 4). IAA14, IAA9, IAA6,
and IAA 26 were the most highly expressed genes in both AZs.
All IAA-related genes were down-regulated in both AZs within
2 h following abscission induction, except for IAA6, IAA14,
and IAA26, whose expression in the FAZ was reduced after 8
The present research compared for the first time the FAZ with
the LAZ, showing similar changes in auxin-related genes in
both AZs. Additionally, the results show that Aux/IAA genes
are the best markers for determining auxin depletion in the
AZs, and that the polar and intracellular auxin transport mechanisms are impaired after auxin depletion. Several IAA-related
genes were shown for the first time to be involved in the abscission process, including PILS, PIN5, REV, and SAUR
10
genes. Taken together, the new data expand the range of various IAA-related genes that are rapidly down-regulated in the
tomato AZs following auxin depletion as a result of flower removal or leaf deblading. Several recent articles further expanded the previously suggested model [74**] for the sequence of
events leading to pedicel abscission following artificial auxin
depletion in tomato flowers. The new data were based on functional analyses of few target genes including KD1, TPRP,
SlERF52, and LX, whose silencing by virus-induced gene silencing, antisense or RNAi delayed abscission. Thus, the early
events following auxin depletion include down-regulation of
IAA-related genes encoding PAT components, auxin carriers,
KD1, and TPRP, while the late events include up-regulation of
ethylene-related genes, such as SlERF52. These lead in turn to
activation of cell wall hydrolyzing enzymes and PCD processes,
which coincided with the increased expression of genes encoding cell wall degrading enzymes and up-regulation of LX, respectively. All these events finally result in the execution of
pedicel or petiole abscission and formation of a protective defense layer on the remaining tissue.
Conclusions
This review provides evidence that auxin depletion in the AZs
is required for AZ cells to react to ethylene as an abscission
signal. This is a general phenomenon that occurs in natural
abscission, in abscission induced by various stresses, and in the
artificial system of tomato organ abscission after removal of the
auxin source. The stress-induced auxin depletion is mediated by
three main intermediate modulators, ethylene, ROS, and carbohydrate starvation. Auxin depletion can result from decreased
IAA biosynthesis and transport, accelerated ATA, and increased oxidative IAA catabolism and conjugation. More target
genes for functional analysis were elucidated by transcriptomic
studies, using NGS or microarray in different abscission systems. The artificial auxin depletion system in tomato was found
to be a very useful system for elucidating the sequence of
events leading to organ abscission.
Direction for future research

In this stage of abscission research, with multiple target genes
that might affect the abscission process, five future research
directions are necessary: 1) performing transcriptomic analyses
with more time points following abscission induction by auxin
depletion, similar to those performed for the tomato FAZ; 2)
analyzing the full transcriptome of the tomato LAZ for elucidating the sequence of events as in the tomato FAZ; 3) continuing the functional analyses of more target genes found in various abscission systems; 4) evaluating the importance of PIN5
and PILS genes family members for auxin signaling in the nucleus of the AZ cells for abscission regulation at the cellular
level; 5) establishing a proteomic system to elucidate the changes in proteins occurring in the AZs following auxin depletion,
and examine if these changes are related to the changes of their
gene expression.
Acknowledgements
Contribution No. 723/15 from the ARO, The Volcani Center,
Bet Dagan, Israel. The authors would like to acknowledge the
support from the United StatesIsrael Binational Agricultural
Research and Development Fund (BARD) [grant no. US-457112C], and the Chief Scientist of the Israeli Ministry of Agricul-
ture Fund [grant no. 203-0898-10]. SS would like to thank the

Indian Council of Agricultural Research for providing him with
an International Fellowship (ICAR-IF), as partial support of his
PhD studies.
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64 Meir S, Hunter DA, Chen J-C, Halaly V and Reid MS. Molecular changes
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65 Liu X, Hegeman AD, Gardner G and Cohen JD. Protocol: High-throughput
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66 Cohen JD, Bausher MG, Bialek K, Buta JG, Gocal GFW, Janzen LM, Pharis
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67 Michaeli R, Riov J, Philosoph-Hadas S and Meir S. Chilling-induced leaf abscission of Ixora coccinea plants. II. Alteration of auxin economy by oxidative
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68 Michaeli R, Philosoph-Hadas S, Riov J, Shahak Y, Ratner K and Meir S.
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69 Wang Y, Li T, Hanyong Meng H and Sun X. Optimal and spatial analysis of
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** An important article describing the role of ARF during tomato flower abscission.
The article includes determination of IAA levels by analytical measurements and by
using the auxin reporter P5::GUS.
70 Guan X, Tao Xu T, Gao S, Qi M, Wang Y, Liu X and Li T. Temporal and
spatial distribution of Auxin Response Factor genes during tomato flower abscission. Journal of Plant Growth Regulation 2014: 33:317-327.
71 Ma C, Meir S, Xiao L, Tong J, Liu Q, Reid MS and Jiang C-Z. A KNOTTED1-LIKE HOMEOBOX protein regulates abscission in tomato by modulating the auxin pathway. Plant Physiology 2015: 167:844853.
** An important article elucidating the function of KD1 in auxin transport during
flower and leaf abscission. The article also includes a visible demonstration of the
12
auxin gradient in the flower pedicel and the flower AZ.

72 Guinn G, Brummett DL. Changes in free and conjugated indole 3-acetic acid
and abscisic acid in young cotton fruits and their abscission zones in relation to
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73 Cai S and Lashbrook CC. Stamen abscission zone transcriptome profiling
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74 Meir S, Philosoph-Hadas S, Sundaresan S, Selvaraj KSV, Burd S, Ophir R,
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auxin depletion. Plant Physiology 2010: 154:1929-1956.
** An intensive study showing changes in gene expression in the AZ and NAZ
during various time-points following auxin depletion by flower removal, and in
response to 1-MCP and IAA application. This study served as the basis for the
suggested detailed sequence of events operating from abscission initiation until the
abscission execution.
75 Agusti J, Merelo P, Cercs M, Tadeo FR and Taln M. Comparative transcriptional survey between laser-microdissected cells from laminar abscission zone
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76 Nakano T, Fujisawa M, Shima Y and Ito Y. Expression profiling of tomato
pre-abscission pedicels provides insights into abscission zone properties including competence to respond to abscission signals. BioMed Central Plant
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** This study reveals at anthesis a region-specific gene expression in the tomato
flower AZ and NAZ (proximal and distal regions to AZ).
77 Wang X, Liu D, Li A, Sun X, Zhang R, Wu L, Liang Y and Mao L. Transcriptome analysis of tomato flower pedicel tissues reveals abscission zone-specific
modulation of key meristem activity genes. PLoS ONE 2013: 8:e55238.
78 Gil-Amado JA and Gomez-Jimenez MC. Transcriptome analysis of mature
fruit abscission control in olive. Plant and Cell Physiology 2013: 54:244-269.
*This study describes a transcriptomic analysis in the AZ during mature olive fruit
abscission.
79 Corbacho J, Romojaro F, Pech J-C, Latch and Gomez-Jimenez MC. Transcriptomic events involved in melon mature-fruit abscission comprise the
sequential induction of cell-wall degrading genes coupled to a stimulation of
endo and exocytosis. PLoS ONE 2013: 8(3):e58363.
* A description of a transcriptomic analysis in the AZ during abscission of mature
melon fruit.
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112 Vandenbussche F, Smalle J, Le J, Jos N, Saibo M, De Paepe A, Chaerle L,
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effects on auxin biosynthesis, transport, and signaling.
115 Rahman A. Auxin: A regulator of cold stress response. Physiologia Plantarum
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124 Tognetti VB, per Mhlenbock P and Van Breusegem F. Stress homeostasis
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** An excellent review summarizing ROS effects on auxin depletion.

140 Xia X-J, Zhou Y-H, Shi K, Zhou J, Christine H. Foyer C-H and Yu J-Q.
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** A very nice demonstration showing how carbohydrate starvation causes auxin
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Stewart Postharvest Review 2015, 2:2

Role of auxin depletion in abscission control

*Correspondence to: Shimon Meir; Email: shimonm@volcani.agri.gov.il

2015 SPS (UK) Ltd.

It is well established that plant hormones apart from auxin and

Meir et al. / Stewart Postharvest Review 2015, 2:2

Auxin Response Factor

Regulation of auxin levels in plants: biosynthesis,

Meir et al. / Stewart Postharvest Review 2015, 2:2

Auxin depletion during natural and

Determination of IAA levels

IAA depletion during senescence-induced flower abscission

Meir et al. / Stewart Postharvest Review 2015, 2:2

unfertilized or male flowers may be ascribed to the low levels of

IAA depletion during senescence-induced leaf abscission

IAA depletion during ripening-induced fruit abscission

Meir et al. / Stewart Postharvest Review 2015, 2:2

Plant and abscission system

Mechanisms for auxin depletion

Apple fruitlets in clusters

Decrease in PAT; decrease in ATA

13, 16, 17, 143, 157

Grapevine berries in clusters

Decrease in PAT; decrease in ATA

Cowpea flowers and fruitlets

Decrease in PAT; decrease in ATA

Bell pepper flowers and fruitlets

Decrease in IAA level , decrease in PAT

Chilling + high light

Increase in IAA oxidation

Cotton buds, flowers, and fruits

Decrease in IAA level

Decrease in expression of IAA signaling genes

Decreased expression of IAA signaling genes

Balsam fir needles

Decrease in IAA level

reduction of endogenous auxin levels, which in turn result in

IAA depletion during self-pruning of spring shoots in

Ethylene as a mediator of IAA depletion

modes of action were suggested for this negative interaction.

Auxin depletion during stress-induced abscission

Meir et al. / Stewart Postharvest Review 2015, 2:2

Meir et al. / Stewart Postharvest Review 2015, 2:2

and data showing that different abscission-related processes

on the transcriptomic results following the application of the

To further define auxin-relevant members of tomato LAZ and

Meir et al. / Stewart Postharvest Review 2015, 2:2

Meir et al. / Stewart Postharvest Review 2015, 2:2

Meir et al. / Stewart Postharvest Review 2015, 2:2

auxin depletion. Interestingly, it was recently reported that over

The highly expressed GH3 genes significantly decreased after

Six ARF genes were exclusively expressed in the FAZ and

Meir et al. / Stewart Postharvest Review 2015, 2:2

Direction for future research

ture Fund [grant no. 203-0898-10]. SS would like to thank the

Meir et al. / Stewart Postharvest Review 2015, 2:2

plants, Journal of Plant Growth Regulators 1983: 2:7380.

Sachs, T. Cell polarity and tissue patterning in plants. Development 1991:

Meir et al. / Stewart Postharvest Review 2015, 2:2

auxin gradient in the flower pedicel and the flower AZ.

Meir et al. / Stewart Postharvest Review 2015, 2:2

** An excellent review summarizing ROS effects on auxin depletion.