Next Article in Journal
Towards Understanding the Decomposition/Isomerism Channels of Stratospheric Bromine Species: Ab Initio and Quantum Topology Study
Previous Article in Journal
Understanding FRET as a Research Tool for Cellular Studies
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 16
Issue 4
10.3390/ijms16046757
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

In Silico Analysis of the Genes Encoding Proteins that Are Involved in the Biosynthesis of the RMS/MAX/D Pathway Revealed New Roles of Strigolactones in Plants

by
Marek Marzec
1,* and
Aleksandra Muszynska
2
1
Department of Genetics, Faculty of Biology and Environmental Protection, University of Silesia, Katowice 40-032, Poland
2
Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben 06466, Germany
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2015, 16(4), 6757-6782; https://doi.org/10.3390/ijms16046757
Submission received: 26 January 2015 / Accepted: 23 March 2015 / Published: 25 March 2015
(This article belongs to the Section Physical Chemistry, Theoretical and Computational Chemistry)
Browse Figures
Versions Notes

Abstract

:
Strigolactones were described as a new group of phytohormones in 2008 and since then notable large number of their functions has been uncovered, including the regulation of plant growth and development, interactions with other organisms and a plant’s response to different abiotic stresses. In the last year, investigations of the strigolactone biosynthesis pathway in two model species, Arabidopsis thaliana and Oryza sativa, resulted in great progress in understanding the functions of four enzymes that are involved in this process. We performed in silico analyses, including the identification of the cis-regulatory elements in the promoters of genes encoding proteins of the strigolactone biosynthesis pathway and the identification of the miRNAs that are able to regulate their posttranscriptional level. We also searched the databases that contain the microarray data for the genes that were analyzed from both species in order to check their expression level under different growth conditions. The results that were obtained indicate that there are universal regulations of expression of all of the genes that are involved in the strigolactone biosynthesis in Arabidopsis and rice, but on the other hand each stage of strigolactone production may be additionally regulated independently. This work indicates the presence of crosstalk between strigolactones and almost all of the other phytohormones and suggests the role of strigolactones in the response to abiotic stresses, such as wounding, cold or flooding, as well as in the response to biotic stresses.

1. Introduction

Strigolactones are a hormone group that has been intensively studied during the last few years. Although they were originally described as an inductor for the germination of the seeds of parasites [1], they were gradually determined to play a role in the signaling between plants and other organisms, such as fungi [2] or bacteria [3], as well as in plant growth and development. The first reports that indicated that strigolactones were negative regulators of the branching of the aboveground part of plants were published in 2008 [4,5]. Subsequent analyses revealed additional functions of strigolactones in plant growth, which included the regulation of the root system development [6,7], the elongation of the mesocotyl and stem [8,9], secondary growth [10], and shoot gravitropism [11]. Participation in plant growth and development processes appears to be a universal role of strigolactones among different species, including both mono- and dicotyledonous plants (reviewed by [12,13,14]).
Additionally, the role of strigolactones in the adaptation to abiotic stresses, mainly in response to nutrient stress, including phosphorus (P) and nitrogen (N) deficiency, has been proposed [15,16]. It was shown that plants increased the production and the exudation of strigolactones in conditions of P and N starvation [17,18,19,20], which allowed the symbiosis with arbuscular mycorrhizal fungi or N-fixing rhizobial bacteria to be enhanced and the development program to be adapted in order to promote the most efficient use of the available resources (reviewed by [21]). The importance of strigolactones in conditions of dehydration stress, including salt and drought stress, has also been proposed. Plants under salt stress increased exudation of strigolactones and additionally strigolactone-deficient or strigolactone-response mutants were hypersensitive to both drought and salt stress [22,23,24].
Significant progress has been made in uncovering the mechanism of strigolactone biosynthesis in the last few years and it now appears that the main players that are involved in this process are known. Strigolactones are carotenoid derivatives that are synthesized in roots that belong to lactones and are composed of four rings (A–D)—a tricyclic lactone core (the ABC part) and a butenolide moiety (the D ring) [25,26]. The C–D part is conserved among the strigolactones that have already been described, while the A–B rings are subjected to modifications, including the substitution of the methyl, hydroxyl and acetyloxyl groups [27,28]. Strigolactone biosynthesis is localized in the chloroplasts, in which three of four enzymes that are already known to be involved in this process are active (Figure 1a). The first one is the carotenoid isomerase D27 (DWARF27), which is an iron-containing protein that is able to convert all-trans-β-carotene into 9-cis-β-carotene [29]. This carotenoid isomerase is encoded by the D27 (Os11g0587000) and AtD27 (At1g03055) genes that were identified in Oryza sativa (rice) [30] and Arabidopsis thaliana [31], respectively. The product of the activity of the D27 isomerase is immobile and it is a substrate for the next stages of strigolactone production, which are conducted by the carotenoid cleavage dioxygenases (CCDs). The first one, CCD7, is a stereo-specific dioxygenase that cleaves to only 9-cis-β-carotene to produce 9-cis-β-apo-10'-carotenal, which is subsequently cleaved by CCD8 to produce carlactone (Figure 1a). Genes that encode both CCDs have been identified in many different plant species, including primitive moss [32,33]. Analyses of Arabidopsis and rice plants that have mutations in the genes that encode CCD7 (MAX3—At2g42620; D17/HTD1—Os04g0550600) and CCD8 (MAX4—At4g32810—D10, Os01g0746400) revealed a highly-branched phenotype, which is characteristic for strigolactone mutants that was reversible after treatment with a strigolactone analogue [5,34,35,36,37] (Figure 1b).
Ijms 16 06757 g001 1024
Figure 1. Strigolactone biosynthesis. (a) Scheme of the biosynthesis pathway divided into four steps and (b) genes encoding proteins that are involved in each stage of this process in Arabidopsis and rice.
Figure 1. Strigolactone biosynthesis. (a) Scheme of the biosynthesis pathway divided into four steps and (b) genes encoding proteins that are involved in each stage of this process in Arabidopsis and rice.
Ijms 16 06757 g001
The structure of carlactone is similar to the one that has been described for strigolactones, because it consists of a C19-skeleton and a C14-moiety, which corresponds to the D-ring of strigolactones [29]. Moreover, carlactone exhibits biological activity that is similar to that of strigolactones, including promoting the germination of the seeds of parasites or regulating shoot branching [29,38]. The presence of carlactone in plants as well as its role as a putative intermediate in strigolactone biosynthesis was confirmed for the first time in 2014. Using 13C-labeled carlactone, the authors proved the conversion of this compound into (–)-[13C]-2'-epi-5-deoxystrigol and 13C-orobanchol, which are the two main precursors of other strigolactones [39]. This conversion, which includes the oxidation of two carlactone positions followed by dehydrogenation [29], is mediated by the last enzyme from the strigolactone biosynthesis pathway, monooxygenase MAX1, which belongs to the cytochrome P450 family. MAX1 was originally characterized in Arabidopsis (At2g26170) and for a long time its function remained unknown, but grafting experiments have suggested that MAX1 acts downstream of both CCDs [40]. Further analysis revealed five MAX1 homologues in rice (Figure 1b), but two of them (Os01g0700900, Os01g0701400) were only present in highly tillered rice varieties that were low strigolactone producers (e.g., cv. Azucena) and that the deletion of these two MAX1 homologues on chromosome 1 was associated with the natural variation of strigolactone biosynthesis in rice [41]. In the next published report, the biochemical function of two rice MAX1 homologues was characterized—Os01g0700900 catalyzes the oxidation of carlactone to produce the first strigolactone ent-2'-epi-5-deoxystrigol, whereas Os01g0701400 is involved in the production of orobanchol via the hydroxylation of the ent-2'-epi-5-deoxystrigol, and thus plays a role in the structural diversification of strigolactones [42]. As was mentioned for Arabidopsis, only one gene encoding MAX1 is present, and recently it was proven experimentally that this monooxydase converts carlactone into carlactonoic acid (9-desmethyl-9-carboxy-carlacton) [43]. Additionally, using the strigolactone pathway in Arabidopsis that was reconstructed in Nicotiana benthamiana, it was shown that MAX1 is not able to produce orobanchol, but only small amount of epi-5-deoxystrigol and 5-deoxystrigol [42]. There are no close homologues of MAX1 in the Arabidopsis genome and questions about other enzymes that may be involved in the production of different strigolactones from 5-deoxystrigol in this species remains unanswered.
The new reports on the multiple functions of strigolactones in plant growth and development, as well as in stress responses or crosstalk with other hormones, have indicated that there might still be some uncovered roles of strigolactones in plants. Because the genetic background of the strigolactone biosynthesis pathway seems to be well studied and increased production of these hormones during responses to different stress stimuli has been described, in silico analyses of genes encoding proteins that are involved in strigolactone biosynthesis may shed a new light on the roles that strigolactones play in plants. In the presented work, we analyzed the sequences of genes that are involved in strigolactone production in two model species Arabidopsis and rice in an attempt to determine new potential functions of strigolactones.

2. Results

2.1. Analysis of the Promoter Sequences of the Arabidopsis Genes that Are Involved in Strigolactone Biosynthesis

Analysis of the promoter sequences of four genes (AtD27, MAX1, 3 and 4), which encode the proteins that are involved in strigolactone biosynthesis in Arabidopsis revealed 55 different motifs for the binding of transcription factors (TFs) (Table 1). The highest number of different TF motifs and their repeats was observed for the promoter of MAX3 (46 and 143, respectively). A similar number of binding sites for TFs was found in the promoters of MAX1 and MAX4 (30 and 34, respectively), but the greatest number of individual binding sites was observed in the MAX4 promoter in comparison to MAX1 (131 vs. 96). The lowest number of TF motifs was found in the promoter of AtD27 (26 TF families and 94 motif repeats). Among the TF families that were identified, the greatest number of them were related to hormonal regulation (26), abiotic stresses (23) and plant growth and development (19), whereas the TFs that are involved in the response to light (12), biotic stresses (7) and metabolism (6) were low (Figure 2a). The largest class of cis-regulatory elements that were identified, which were related to hormonal regulation, can be divided into specific phytohormone subgroups, such as abscisic acid (15), auxin (7), brassinosteroid (1), cytokinin (2), ethylene (6), gibberellin (4) jasmonic acid (4) and salicylic acid (8) (Figure 2b). Among the TFs that are involved in the responses to abiotic stresses, those related to salt (16), drought (11), low temperatures (9), wounding (6), nutrients (4), flooding (1) and osmotic stress (1) can be distinguished (Figure 2c), while the biotic stresses category can be divided according to pathogens, such as viruses (1), bacteria (4), fungi (4), insects (1) or xenobiotics (2).
Table
Table 1. Motifs for TFs and their number, which were found in the promoter sequences of genes encoding proteins in Arabidopsis that are involved in strigolactone biosynthesis.
Table 1. Motifs for TFs and their number, which were found in the promoter sequences of genes encoding proteins in Arabidopsis that are involved in strigolactone biosynthesis.
TFs MotifsAtD27MAX3MAX4MAX1Gene Ontology (GO) Process
AGL31444growth and development
AG3464growth and development
ATHB-1911146abiotic stresses (salt, nutrients); growth and development; response to light
ATHB-591088hormonal regulation (ABA)
ATHB-95797growth and development
RAV1-A/RAV1AAT5613growth and development; hormonal regulation (BR); metabolism
ACGTATERD141062abiotic stresses (drought, salt); response to light
ANAERO1-3CONSENSUS2131abiotic stresses (flooding)
ARR105352growth and development; hormonal regulation (CYT)
ARR1AT717106growth and development; hormonal regulation (CYT); metabolism
ASF1MOTIFCAMV1221biotic stresses ( bacteria, xenobiotics); hormonal regulation (IAA, SA); response to light
Bellringer1123growth and development
GATABOX1010185abiotic stresses (nutrients); response to light
GT1CONSENSUS9589response to light
MYB1AT3413abiotic stresses (drought, salt)
MYCCONSENSUSAT6869abiotic stresses (drought, salt); hormonal regulation (ABA)
MYB42215abiotic stresses (wounding); hormonal regulation (JA, SA); metabolism
SURECOREATSULTR112111abiotic stress (nutrients)
WBOXATNPR13331biotic stresses (bacteria, fungi, viruses); hormonal regulation (SA)
CDC51010biotic stresses (bacteria, fungi); growth and development
PIF30210response to light; hormonal regulation (GB)
ABRE-like0200abiotic stresses (cold, drought, salt)
ABREATCONSENSUS0100abiotic stresses (cold, drought, salt); hormonal regulation (ABA)
ABRELATERD10110abiotic stresses (cold, drought, salt); response to light
ABRERATCAL0010abiotic and biotic stresses (induced by Ca2+); hormonal regulation (ABA)
ABRE0100hormonal regulation (ABA)
ACGTABREMOTIFA2OSEM0100hormonal regulation (ABA)
AP10121growth and development
ARFAT/ARF1100growth and development; hormonal regulation (IAA)
Agamous0113growth and development
AtMYB20100abiotic stresses (cold, nutrients, salt, wounding); hormonal regulation (ABA, ET, IAA, JA, SA)
AtMYC20110abiotic stresses (wounding); biotic stresses ( fungi, insects); hormonal regulation (ABA, JA, SA); metabolism
C8GCARGAT0440growth and development; hormonal regulation (IAA); metabolism
CGCGBOXAT0040abiotic stresses (low temperatures, salt, wounding); hormonal regulation (ET, IAA)
CCA1ATLHCB1/CCA11001abiotic stresses (low temperatures, salt); hormonal regulation (ABA, ET, GB, IAA, SA)
DPBFCOREDCDC30100abiotic stresses (drought, low temperatures, salt); biotic stresses (fungi); hormonal regulation (ABA, GB)
GAREAT0113hormonal regulation (GB)
GBF50200biotic stresses (xenobiotics); growth and development
LEAFYATAG0001growth and development
LTREATLTI780100abiotic stresses (low temperatures)
LTRECOREATCOR150100abiotic stresses (low temperature); response to light
MYB1LEPR0101biotic stresses ( bacteria); hormonal regulation (ET)
MYB2CONSENSUSAT0101abiotic stresses (drought, salt); hormonal regulation (ABA)
MYBATRD220100abiotic stresses (salt, wounding); hormonal regulation (ABA, ET, IAA, SA)
MYBCORE0111abiotic stresses (drought, salt, wounding); hormonal regulation (ABA, ET, IAA, JA, SA)
MYBPLANT1012abiotic stresses (drought, salt); hormonal regulation (ABA); metabolism
MYCATERD1/MYCATRD220110abiotic stresses (drought, salt); hormonal regulation (ABA)
PREATPRODH0200abiotic stresses (osmotic)
SITEIIATCYTC0001growth and development; metabolism
SORLIP5AT1100response to light
SREATMSD0100growth and development
SV40COREENHAN1101response to light
TBOXATGAPB1020response to light
ZDNAFORMINGATCAB10100growth and development; response to light
XYLAT0010growth and development
One TF can be involved in different processes and therefore it has been assigned to different categories. The binding sites that are underlined were identified in the promoter sequences of all of the Arabidopsis genes that were analyzed; ABA—abscisic acid; BR—brassinosteroid; CYT—cytokinin; ET—ethylene; GB—gibberellin; IAA—auxin; JA—jasmonic acid; SA—salicylic acid.
Ijms 16 06757 g002 1024
Figure 2. Categories of the processes that are regulated by the TFs that have binding sites in the promoter sequences of genes encoding proteins that are involved in strigolactone biosynthesis. (a) The six main categories of the processes that are regulated by the TFs that were identified; (b) detailed information about the TFs that are involved in hormonal regulation; (c) the number of TF families that are related to different abiotic; and (d) biotic stresses.
Figure 2. Categories of the processes that are regulated by the TFs that have binding sites in the promoter sequences of genes encoding proteins that are involved in strigolactone biosynthesis. (a) The six main categories of the processes that are regulated by the TFs that were identified; (b) detailed information about the TFs that are involved in hormonal regulation; (c) the number of TF families that are related to different abiotic; and (d) biotic stresses.
Ijms 16 06757 g002
Special attention should be paid to those of the 19 TF families (34.5% of the total number that were identified) that were found in the promoter sequences of all of the Arabidopsis genes that were analyzed (Table 1). Among them, representatives of each of the described categories of biological processes were observed: abiotic and biotic stresses, growth and development, hormonal regulation, metabolism, as well as response to light. The highest number of repeated motifs were identified for GATABOX (43 in total), ATHB-1 (40 in total), ARR1AT (40 in total), ATHB-5 (37 in total) and GT1CONSENSUS (31 in total). The presence of those cis-regulatory elements in the promoter sequences of all known genes encoding proteins that are known to be responsible for strigolactone biosynthesis indicate that strigolactones may be involved in the processes that are regulated by the described TFs. On the other hand, the presence of binding sites of TFs that are specific to only individual genes could mean that the different stages of strigolactone production have their own mechanisms of regulation. Interestingly, specific TF motifs were not observed in only the AtD27 promoter sequence, whereas for the other genes, MAX1, MAX3 and MAX4, a different number of specific cis-regulatory elements were identified (1, 4 and 2, respectively).
The highest similarity in the cis-regulatory motifs was found between AtD27 and MAX1 (64.7%; 22 motifs out of 34), but the highest number of binding sites was shared by two genes encoding carotenoid cleavage dioxygenases—MAX3 and MAX4 (28 families out of 52; Table 2). The lowest level of similarity in the TFs that can bind in the promoter region was observed for AtD27 and MAX3 (44%, 22 TF families out of the 50 that were identified).
Table
Table 2. The similarity of TF binding sites that were found in the promoter sequences of the genes encoding proteins in Arabidopsis that are involved in strigolactone biosynthesis.
Table 2. The similarity of TF binding sites that were found in the promoter sequences of the genes encoding proteins in Arabidopsis that are involved in strigolactone biosynthesis.
-D27MAX3MAX4MAX1
D27-44% (22/50)55.3% (21/38)64.7% (22/34)
MAX344% (22/50)-53.8% (28/52)52% (26/50)
MAX455.3% (21/38)53.8% (28/52)-58.5% (24/41)
MAX164.7% (22/34)52% (26/50)58.5% (24/41)-

2.2. Analysis of the Promoter Region of the Rice Genes that Are Involved in Strigolactone Biosynthesis

Analysis of the promoter region of four rice genes encoding proteins involved in strigolactone biosynthesis revealed binding sites for 18 TFs families, whereof six were present in each promoter sequence (Table 3). Some of the rice motifs, like AMYBOX1 or CGACGOSAMY3, could not be assigned to the one of previously established groups of biological processes and in this case the descriptive information about their function was included. Among TFs that can interact with all of the genes that were analyzed were representatives of all of the biological processes: abiotic and biotic stresses, growth and development, hormonal regulation, metabolism and response to light were present. However, their number was lower in comparison to those identified for Arabidopsis genes. Interestingly, almost all of TF motifs described for D27 (6 from 7) and for OsMAX1 (6 from 9) were shared with other genes involved in strigolactone biosynthesis in rice (Table 3). The most frequently occurring cis-regulatory elements represented in all genes that were analyzed were: WRKY71OS (30 in total), GT1CONSENSUS (28 in total) and GATABOX (25 in total), which are related to the response to abiotic stresses, hormonal regulation and the response to light.
Some cis-regulatory elements were observed in the promoter sequences of all of the Arabidopsis and rice genes that were analyzed (GATABOX, GT1CONSENSUS) and additionally those binding sites were repeated several times in each gene of both species.
Table
Table 3. TF motifs found in the promoter sequences of rice genes encoding proteins that are involved in strigolactone biosynthesis.
Table 3. TF motifs found in the promoter sequences of rice genes encoding proteins that are involved in strigolactone biosynthesis.
TF MotifsD27D17/HTD1D10MAX1Gene Ontology (GO) Process
BIHD1OS2214biotic stresses (fungi)
GATABOX10735abiotic stresses (nutrients); response to light
GT1CONSENSUS71227hormonal regulation (SA); response to light
PYRIMIDINEBOXOSRAMY1A1212hormonal regulation (GB); growth and development; sugar repression
SITEIIATCYTC1222growth and development; metabolism; Relative to cytochrome, oxidative phosphorylation
WRKY71OS66612biotic stresses (pathogens); hormonal regulation (GB)
ABREOSRAB210110hormonal regulation (ABA); abiotic stresses (osmotic)
ACGTABOX0260growth and development; sugar repression
ANAERO1-3CONSENSUS0101abiotic stresses (flooding)
ARFAT0100growth and development; hormonal regulation (IAA)
AMYBOX10010Conserved sequence found in 5'-upstream region of alpha-amylase gene
E2FCONSENSUS0100growth and development
CAREOSREP10010hormonal regulation (GB)
CGACGOSAMY30040Conserved sequence found in 5'-upstream region of alpha-amylase gene
GARE1OSREP10020hormonal regulation (GB)
HEXMOTIFTAH3H40102hormonal regulation (IAA, SA); metabolism
TATABOXOSPAL0101abiotic stresses (salt); hormonal regulation (ET, GB, IAA, JA, SA)
TATCCAOSAMY2000abiotic stresses ( nutrients); hormonal regulation (GB); found in alpha-amylase promoters of rice
One TF can be involved in different processes and therefore it has been assigned to different categories. The binding places for the TFs that are underlined were observed in the promoter sequences of all of the rice genes that were analyzed; ET—ethylene; GB—gibberellin; IAA—auxin; JA—jasmonic acid; SA—salicylic acid.

2.3. Identification of miRNA Target Sites in the mRNAs of Genes from the Strigolactone Biosynthesis Pathway

At least one target site for eight different miRNAs were identified in MAX1, MAX3 and MAX4. In MAX3 and MAX4 one target site, which was complementary to nine different miRNAs, was identified, whereas for MAX1, two target sequences that were recognized by 20 miRNAs were identified. The target sequences for seven different miRNAs (ath-miR165b; ath-miR166a-g) were found in the mRNA of all three MAX genes. Additionally, the mRNA of MAX1 and MAX3 contains sequences that were recognized by the miRNAs that were specific only to them (Table 4).
A large number (69) of target sequences for different miRNAs were identified in the mRNA of four rice genes encoding proteins of the strigolactone biosynthesis pathway. Among them, only three were present in all of the genes: osa-miR444, osa-miR528 and osa-miR531. However, osa-miR531 was also annotated as repetitive sequences [44] and this was the reason why it was excluded from a detailed analysis (Table 4). Additionally, mRNA of D17/HTD1, D10 and OsMAX1 were recognized by the miRNAs that are specific only for them (17, 18 and 4 miRNAs, respectively).
Table
Table 4. Target sites for the miRNA that was found in the mRNA of Arabidopsis and rice genes encoding proteins that are involved in the strigolactone biosynthesis.
Table 4. Target sites for the miRNA that was found in the mRNA of Arabidopsis and rice genes encoding proteins that are involved in the strigolactone biosynthesis.
miRNAPosition of Target Sites
Arabidopsis Genes
AtD27MAX3MAX4MAX1
ath-miR156g---302–323
ath-miR165a--950–971842–861
ath-miR165b-1469–1493950–971842–861
ath-miR166a-g-1469–1493951–971842–861
1280–1301
ath-miR395b,c,f---336–357
ath-miR401-1701–1725--
-Rice Genes
D27D17/HTD1D10OsMAX1
osa-miR44447–70557–581172–154458–478
1055–1076
363–380221–239
1292–1318
osa-miR52814–33363–380 1192–1214331–351
864–8851113–1138

2.4. Gene Expression after Hormone Treatment and during Responses to Abiotic Stresses

The effect of different hormone treatments on gene expression was checked for all of the Arabidopsis genes that are responsible for the strigolactone biosynthesis pathway. There is no universal response in the expression of all of the genes that is induced by abscisic acid, auxin, brassinolide, cytokinin, ethylene, gibberellin acid or methyl jasmonate. Moreover, for some of the genes that were analyzed, the opposite effect (induction or repression) was observed at different time points during treatment with the same hormone (Table 5). However, in some cases the same effect was caused by a hormone at all of the time points, i.e., the induction of MAX3 was observed during ethylene treatment; abscisic acid, auxin and brassinolide increased the expression of MAX4; the transcription of MAX1 was enhanced by brassinolide and was inhibited by auxin, cytokinin, gibberellin acid and methyl jasmonate treatment (Table 5).
Table
Table 5. Relative level of Arabidopsis genes expression in roots after treatment with different hormones.
Table 5. Relative level of Arabidopsis genes expression in roots after treatment with different hormones.
TreatmentTime Pointlog2 Ratio (Sample Signal/Control Signal)
AtD27MAX3MAX4MAX1
Abscisic acid (10 µM)0.5 h0.01−0.270.23−0.15
1 h0.440.040.23−0.39
3 h−0.560.830.230.05
Auxin (IAA 1 µM)0.5 h0.15−0.190.3−0.04
1 h−0.22−0.541.34−0.38
3 h−0.240.240.58−0.52
Brassinolide (10 nM)0.5 h0.56−0.351.050.07
1 h−0.05−0.71.070.04
3 h−0.30.10.120.15
Cytokinin (zeatin 1 µM)0.5 h−0.1−0.05−0.04−0.43
1 h0−0.030.72−0.76
3 h−0.330.37−0.39−0.45
Ethylene (ACC 10 µM)0.5 h0.450.060.8−0.04
1 h0.340.040.67−0.07
3 h−0.630.55−0.260.09
Gibberellin acid (1 µM)0.5 h0.13−0.29−0.08−0.11
1 h0.28−0.150.01−0.25
3 h−0.170.44−0.34−0.19
Methyl jasmonate (10 µM)0.5 h0.530.10.48−0.13
1 h−0.37−0.20.37−0.21
3 h−1.20.22−0.2−0.05
Data for seven-day-old seedlings of Arabidopsis, Columbia-0 ecotype, which were obtained from the eFP Browser [45,46] and PathoPlant database [47,48]. The mean values of the log2 ratio for two biological replicates were present; ACC (1-aminocyclopropane-1-carboxylic acid)—an ethylene precursor; IAA (indole-3-acetic acid)—an active form of auxin.
The expression of rice genes was investigated in the case of treatment with abscisic acid, auxin, brassinolide, cytokinin, gibberellin acid or jasmonic acid. The relative levels of D17/HTD1, D10 and OsMAX1 expression changed under treatment with the same hormones; and moreover, some of the hormones diversely regulated the expression of individual genes, depending on the time. An equivalent treatment effect was observed for MAX1 whose expression was induced by abscisic acid, brassinolide or cytokinin and repressed by jasmonic acid; the expression of D10 after treatment with cytokinin and jasmonic acid decreased, while a lower expression level of D17/HTD1 in comparison to control conditions was observed after treatment with brassinolide (Table 6).
Table
Table 6. Relative level of rice genes expression in roots after treatment with different hormones.
Table 6. Relative level of rice genes expression in roots after treatment with different hormones.
TreatmentTime Pointlog2 RatioTreatmentTime Pointlog2 Ratio
D17/HTD1D10MAX1D17/HTD1D10MAX1
Abscisic acid (50 µM)0.25 h0.10−0.070.07Cytokinin (zeatin 1 µM)0.25 h−0.31−0.370.03
0.5 h−0.06−0.220.300.5 h0.26−0.390.71
1 h−0.31−0.150.891 h−0.12−0.280.92
3 h0.260.061.433 h−0.20−0.241.06
6 h0.570.242.326 h−0.17−0.110.79
Auxin (IAA 10 µM)0.25 h0.210.050.21Gibberellin acid (10 µM)0.25 h−0.02−0.44−0.34
0.5 h−0.35−0.170.090.5 h−0.27−0.06−0.66
1 h−0.26−0.380.331 h−0.01−0.12−0.41
3 h1.11−0.060.663 h0.23−0.13−0.63
6 h0.29−0.09−0.026 h−0.120.380.07
Brassinolide (1 µM)0.25 h−0.430.020.15Jasmonic acid (100 µM)0.25 h−0.26−1.65−0.17
0.5 h−0.13−0.130.220.5 h0.90−1.01−0.30
1 h−0.44−0.250.131 h0.79−0.69−0.59
3 h−0.19−0.020.253 h2.46−0.82−0.70
6 h−0.150.020.356 h2.77−0.85−0.87
Data for seven-day-old seedlings of rice, cv. Nipponbare, according to the RiceXPro database [49,50]. Mean values of log2 ratio for three biological replicates were present; IAA (indole-3-acetic acid)—an active form of auxin.
The relative expression levels of the gene-encoding proteins that are involved in strigolactone biosynthesis in Arabidopsis were also analyzed under different abiotic stresses, such as drought, cold, osmotic stress, wounding, salt, heat, UV-B, genotoxic or oxidative stress. None of stress factors that were tested had the same influence in regards to increasing or decreasing the expression of all of the genes from the strigolactone biosynthesis pathway. Moreover, at different time points under the same stress the expression of the genes that were analyzed was modulated in two different ways, which was similar to that observed for the hormone treatment. However, the response of individual genes to some of stress factors was the same: the expression of AtD27 decreased under salt, genotoxic and UV-B stress, while the expression of MAX3 was induced under wounding, heat, UV-B and genotoxic stress conditions (Table 7).
Table
Table 7. Relative level of Arabidopsis gene expression under the response to the different stresses.
Table 7. Relative level of Arabidopsis gene expression under the response to the different stresses.
StressTimeAtD27MAX3MAX4MAX1StressTimeAtD27MAX3MAX4MAX1
Cold0.5 h0.25−0.3−0.470.08Drought0.25 h−1.010.33−0.610.26
1 h−0.080.29−0.10.370.5 h−0.15−0.44−0.28−0.25
3 h0.240.140.050.041 h−0.70.76−0.080.62
6 h0.15−0.930.330.353 h0.030.90.080.01
12 h−0.22−0.820.31−0.876 h0.210.57−0.090.49
24 h−0.04−0.13−0.28−2.2712 h00.360.14−0.03
Osmotic0.5 h0.23−0.24−0.03−0.2824 h−0.550.190.16−0.09
1 h−0.050.62−0.13−0.04Wounding0.25 h−1.360.8−0.09−0.06
3 h−0.111.06−0.01−0.150.5 h0.130.19−0.14−0.02
6 h0.330.720.730.531 h−0.310.52−0.330.39
12 h−0.821.351.60.393 h0.380.42−0.240.08
24 h−0.670.971.40.716 h−0.490.46−0.110.51
Salt0.5 h−0.020.24−0.140.2112 h−1.440.75−0.34−0.14
1 h−0.540.66−0.340.1324 h−0.510.380.24−0.05
3 h−0.350.43−0.03−0.46Heat0.25 h−0.090.450.230.08
6 h−0.36−0.60.38−0.610.5 h0.230.210.030.49
12 h−0.940.181.240.271 h−0.21.17−0.860.09
24 h−0.610.130.42−0.153 h−0.021.65−0.49−0.55
Genotoxic0.5 h−0.230.15−0.150.014 h0.050.20.530.46
1 h−1.160.64−0.190.146 h−0.550.47−0.18−0.15
3 h−0.590.18−0.45−0.112 h−0.960.950.610.75
6 h−0.510.010.180.1224 h0.20.180.120.19
12 h−0.950.160.460.22UV-B0.25 h−0.340.24−0.25−0.22
24 h−0.110.10.440.090.5 h−0.110.64−0.110.34
Oxidative0.5 h−0.190.18−0.250.011 h−0.681.15−0.960.49
1 h−0.470.42−0.230.223 h−0.260.56−1.01−0.32
3 h0.50.68−0.03−0.246 h−0.360.16−0.550.13
6 h−0.520.41−0.340.0412 h−0.570.29−0.220.22
12 h−0.4−0.10.480.0624 h−0.530.20.07−0.12
24 h−0.270.420.550.51-----
Data for seven-day-old seedlings of Arabidopsis, Columbia-0 ecotype, which were obtained by Kilian and co-workers [51]. Mean values of log2 ratio for two biological replicates were present.

3. Discussion

3.1. Regulation of the Expression of Genes that Are Responsible for Strigolactone Biosynthesis via TFs and miRNAs

To the best of our knowledge, this is the first report describing which TFs may regulate the strigolactone biosynthesis; however, the role of some TFs in the regulation of individual genes related to strigolactone biosynthesis has been postulated previously [52]. TFs play a crucial role in the coordination of plant growth and development, as well in the response to different stresses because they are able to regulate the spatial expression of the many different genes that are contained in the promoter region motifs that are recognized by TFs [53]. Based on the experimental data that describes the role the regulation of gene expression in model species [54,55], it is possible to screen the promoter region of any gene to identify which TFs are able to influence its expression [56,57,58]. Knowledge about which TFs can activate the gene expression allows the function of the gene that was analyzed in plant development program or response to external factors to be predicted.
Plant hormones are involved in many processes during a plant’s life and the genes encoding proteins that are responsible for the biosynthesis or signaling pathway are under the control of different TFs [59,60]. Based on the fact that the binding site for a specific TF is present in the promoter region of all of the genes that are responsible for the biosynthesis pathway of strigolactones, we assumed that strigolactones may be involved in the processes that are regulated by this TF. In the case of Arabidopsis genes, the 19 motifs of cis-regulatory elements were present in the promoter region of all four of the genes that were analyzed and most of them were identified in replicates (Table 1). Among them, the majority is related to processes that were already described as being regulated by strigolactones, such as: plant growth and development (AGL3, AG, ATHB-9, Bellringer) [14]; response to nutrient stress (ATHB-1, GATABOX, SURECOREATSULTR11) [21,61]; response to light (GT1CONSENSUS) [62,63]; or very recently some have been postulated to be involved in the response to drought (like ACGTATERD1, MYB1AT) [23,24]. However, some of the TFs that were identified in the promoter region of all of the Arabidopsis genes that were analyzed are involved in processes that have not yet been linked to strigolactones. The presence of the WBOXATNPR1 and ASF1MOTIFCAMV motifs indicates that the strigolactone biosynthesis pathway may be induced during a response to biotic stresses. Both cis-regulatory elements are bound by the TFs that are induced by salicylic acid [64] and it was confirmed that both TFs play a role in a plant’s defense reaction against viruses, bacteria or fungi [65,66]. Moreover, an analysis of the genes encoding strigolactone biosynthesis pathway in rice revealed the presence of BIHD1OS and WRKY71OS motifs, which are related to defense mechanisms against fungi and other pathogens, in each promoter region [67,68]. This possible new role of strigolactones might be explained by the known connection between arbuscular mycorrhizal symbiosis that is regulated via strigolactones and plant responses to biotic stresses (reviewed by [69]).
The second unexpected process that might be linked to strigolactones that is based on an in silico analysis is their participation in the response to flooding (because of the presence of the ANAERO1-3CONSENSUS motifs). These motifs were found in the promoter region of anaerobically induced genes that are involved in the fermentative pathway [70] and were present in all of the Arabidopsis genes that are known to be responsible for strigolactone biosynthesis as well as in individual rice genes (D17/HTD1 and MAX1). The response to flooding mainly covers cell protection against cytosolic acidification and the accumulation of reactive oxygen species and toxins as well as the activation of the enzymes in the fermentation pathway [71,72]. To the best of our knowledge, there is no literature data to date that indicates a link between strigolactones and a resistance to flooding, and therefore we may speculate that the part of the flood-response that covers plant growth may be regulated by strigolactones. However, our analysis also revealed that a few of the TFs that are involved in the metabolic processes have their binding sites in promoter regions of the genes that were analyzed: in rice these were mainly related to alfa-amylases and sugar (i.e., PYRIMIDINEBOXOSRAMY1A, AMYBOX1, CGACGOSAMY3), whereas in Arabidopsis they were mainly related with fatty acid beta-oxidation, oxidative phosphorylation or polyamine catabolic process (i.e., ARR1AT, MYB4, SITEIIATCYTC), which may be related to the response to flooding (Figure 3).
The gene activity on the post-transcriptional level can be controlled i.e., by miRNAs. miRNAs are short (21–24 nucleotides) molecules, which based on the sequence complementarity join to mRNA, thus resulting in the degradation or repression of translation (reviewed by [73,74]). The miRNAs that repress TFs have the greatest impact on gene expression because through the inactivation of an individual TF, they influence the expression of all of the genes that are regulated via this TF. However, miRNA can not only inhibit the production of TFs, but also other proteins, i.e., from hormone biosynthesis or signaling pathways, such as the auxin receptor that is encoded by TIR1/AFB2 [75]. Moreover, it was shown that miRNAs play a main role in the response to different external factors, such as drought [76] or wounding [77]. In the mRNAs of the genes that were analyzed, target sequences that were recognized by the same miRNAs were present; in Arabidopsis for MAX1, -3 and -4, and in rice for all of the genes. This is a clear indication of the presence of at least one universal post-transcriptional mechanism that is able to inhibit the entire pathway of strigolactone biosynthesis. Moreover, some of the miRNAs that were identified regulate the activity of not only the MAX1, -3 and -4 genes, but also TFs, which induces the expression of some of the genes that were investigated, such as miR165b whose target gene is ATHB9 [78]. Other miRNAs, such as miR166a-g, which recognized the mRNA of MAX1, -3 and -4, have been described as being involved in the regulation of the initiation of the axillary meristem and leaf development, which confirms a role of strigolactones in plant growth that was already known [79]. However, except the miRNAs that repress all of the genes from the strigolactone biosynthesis pathway, some others have only been specific to the particular mRNAs that were analyzed, which indicates that the different stages of strigolactone production have their own mechanisms of post-transcriptional regulation.

3.2. Expression of Strigolactone Biosynthesis Genes after Hormone Treatment and under Stress Conditions

Analysis of the TFs that induced the expression of the strigolactone biosynthesis genes showed a large number of TF families that are related to hormonal regulation. In the case of the Arabidopsis genes (AtD7, MAX1, MAX3 and 4), TFs that are associated with almost all of phytohormones were identified, including abscisic acid, auxin, brassinosteroid, cytokinin, ethylene, gibberellin, jasmonic acid or salicylic acid, whereas the analysis of the rice genes encoding proteins that are involved in strigolactone production revealed that their expression can be regulated via the TFs that are related to auxin, ethylene, gibberellin, jasmonic acid or salicylic acid. The question is whether other hormones may really affect strigolactone production.
Within the last year, a great deal of progress has been made in uncovering the relationships between strigolactones and other hormones; however, many interactions remain unexplained (reviewed by [80]). The best known is the crosstalk between strigolactones, auxin and cytokinin during axillary bud outgrowth. The growth of an axillary bud depends on the export of auxin and strigolactones that can inhibit its polar transport via the disorganization of the arrangement of PIN proteins [81,82], which means that strigolactones and auxin act together to arrest growth of an axillary bud, whereas cytokinin works antagonistically to them and promotes the outgrowth of a bud [83]. Several reports have indicated that auxin may induce the expression of MAX3 and MAX4 in Arabidopsis [84], as well as its homologues in other species, like pea or rice [85,86]. However, an analysis of available microarray data revealed that the auxin treatment of Arabidopsis and rice seedlings affects the expression of the different components of strigolactone biosynthesis pathway differently, including MAX3 and MAX4, and additionally that this effect depends on the time of treatment (Table 4 and Table 5). Similar results were obtained for other hormones; none of the hormones that were analyzed universally affected the entire pathway of strigolactone synthesis in either of the species that were investigated; however, each of them somehow changed the relative expression levels of all of the genes in Arabidopsis and rice that were analyzed. This is a strong confirmation of the roles of the previously identified TFs that are related to hormone regulation.
Ijms 16 06757 g003 1024
Figure 3. Regulation of the expression and post-transcriptional activity of Arabidopsis genes that encode the different stages of strigolactone production; common mechanisms were present for all of the genes that were analyzed and the new predicted functions of this phytohormone class were underlined.
Figure 3. Regulation of the expression and post-transcriptional activity of Arabidopsis genes that encode the different stages of strigolactone production; common mechanisms were present for all of the genes that were analyzed and the new predicted functions of this phytohormone class were underlined.
Ijms 16 06757 g003
One explanation of different effects of hormone treatment on the expression of specific genes from the strigolactone production pathway might be the fact that the different stages of strigolacone production have their own mechanisms of regulation and additionally that strigolactones are tissue-specific [87] or that their functions depend on additional external conditions [13]. The diverse expression of the genes that are involved in strigolatone biosynthesis or the diverse level of the compounds from the strigolactone biosynthesis pathway in a plant’s response to external factor has already been already described. For example, an analysis of two MAX1 homologues in rice revealed that the expression of Os01g0700900 is induced under P starvation, whereas Os01g0701400 expression remained unchanged under the same conditions [41]. This means that of the two enzymes that are involved in the consecutive stages of strigolactone biosynthesis, the production of ent-2'-epi-5-deoxystrigol and orobanchol, respectively [42], only one plays a role in the response to nutrient stress. Moreover, a measurement of carlactone and 5-deoxystrigol levels in Arabidopsis and rice plants that were growing in low P conditions demonstrated that only the level of 5-deoxystrigol was significantly elevated, but that the carlactone level decreased slightly [39,88]. The simplest explanation of experimental and in silico results that are obtained for strigolactone biosynthesis genes expression and the level of strigolactone compounds under different stresses or after hormone treatment is assumed to be that some strigolactone metabolites are stored by plants and constitute a reservoir for the rapid synthesis of their derivatives, which is mediated by individual enzymes in response to stress or hormone treatment.

3.3. In Silico Analysis for the Prediction of New Roles of Strigolactones in Plants

The results that were obtained during an in silico analysis of genes encoding proteins that are involved in strigolactone biosynthesis revealed new, as yet unconfirmed, roles of strigolactones in a plant’s response to biotic and abiotic stresses, as well as new crosstalk between strigolactones and other hormones. Moreover, the studies that are presented confirm the contribution of strigolactones in response to dehydration stresses, which have been described very recently [23,24]. Both reports point out the positive role of strigolactones during drought and salt stresses. Ha and co-workers showed that both strigolactone-deficient (max3-11, max4-7) and signaling (max2-3) mutants were hypersensitive to dehydration and concluded that strigolactones modulate the stress response to drought via abscisic acid-dependent and abscisic acid-independent pathways in Arabidopsis [24]. The studies that were carried out by Bu and co-workers indicate that only the strigolactone-response Arabidopsis mutants (max2-1, max2-2) are hypersensitive to drought, but that the strigolactone-deficient ones (max1, max3, max4) do not differ in comparison to the wild-type, which means that strigolactones are not involved in the abscisic acid response pathway [23]. These differences might result from the different methods that are used for the induction of drought stress and need to be clarified through additional investigations; however, they also indicate that the role of strigolactones in the stress response is heterogeneous and may be restricted only to the biosynthesis/signaling part or to the individual stages of one of those processes. Hence, the results that are presented in this paper, which did not show a universal response in the expression levels of all genes from strigolactone biosynthesis under different treatments, remain consistent with the experimentally generated data. Moreover, in our opinion the link between TFs and the fact that they may affect the transcription level of the genes that were analyzed and change their expression under the different conditions that are related to described TFs is a strong indication that strigolactones play many different roles in plants, which have still not been confirmed experimentally (Figure 3).

4. Experimental Section

4.1. Promoter Analysis

The 1000 bp long promoter sequences of Arabidopsis genes (At1g03055; At2g42620; At4g32810 and At2g26170) were obtained using the PlantPAN analytical resource [89,90], whereas the same length of promoter sequences of rice genes (Os11g0587000; Os04g0550600; Os01g0746400 and Os01g0701500) were found in Rice Annotation Project Database [91]. The promoter sequences that were obtained were analyzed using three databases: AGRIS [92,93], JASPAR [94,95] and PLACE [96,97] in order to find the TF motifs. The list of TF families that were obtained for each gene were compared to each other in order to predict any TFs that were common for the Arabidopsis and rice genes that are involved in strigolactones biosynthesis.
TFs were assigned to the different processes based on the information that are available in the TRANSFAC Database [98,99], the PlantTF Database [100,101] and in the literature. Six main groups of biological processes were created: abiotic stresses, biotic stresses, growth and development, hormonal response, metabolism and response to light (Figure 4).
Ijms 16 06757 g004 1024
Figure 4. Scheme presented the strategy and tools used during analysis. Detailed description was given in the Experimental Section.
Figure 4. Scheme presented the strategy and tools used during analysis. Detailed description was given in the Experimental Section.
Ijms 16 06757 g004

4.2. Identification of the Sequences that Were Recognized by miRNA

The sequences of mRNA for all of the Arabidopsis and rice genes were obtained from the NCBI GeneBank and analyzed using the PlantPAN Database [89,90] in order to identify the target sites for miRNA. The Information about possible role of miRNA in plants was collected via miRBase [102,103] and data from the literature (Figure 4).

4.3. Expression Profiles

The expression of Arabidopsis genes was analyzed using the eFP Browser tool [45,46] and the PathoPlant database [47,48]. For AtD27, MAX3 and MAX1, their TAIR ID was used to explore the databases, whereas for MAX4 its Affymterix Probe ID was used (253398_at). The data for abiotic stresses was obtained from the results that were published by Kilian and co-workers [51] and included cold, osmotic, salt, genotoxic, oxidative, drought, wounding, heat and UV-B stress that had been tested on 18-day-old seedlings of the wild-type Columbia-0 ecotype. The data for hormonal treatment came from the eFP Browser and PathoPlant resources and they include the response to abscisic acid, auxin, cytokinin, ethylene, methyl jasmonate, gibberellin and brassinolide [45,47]. Those data were collected for the roots of seven-day-old seedlings of Arabidopsis thaliana, Columbia-0 ecotype.
Only three rice gene-encoding proteins that are responsible for the strigolactone biosynthesis pathway were assigned to the probes that were analyzed under microarray experiments—D17/HTD1, D10 and OsMAX1 (Os01g0701500). The expression in the roots was investigated under hormonal treatment using abscisic acid, auxin, brassinolide, cytokinin, gibberellin or jasmonic acid and the data was obtained from the RiceXPro Database [49,50]. Analysis was carried out on the roots of seven-day-old seedlings of Oryza sativa L. japonica cv. Nipponbare (Figure 4).
The relative expression level of the genes that were analyzed is presented as the log2 fold change between the control conditions and the different treatment or stress factors. Data for genes of the same species was compared only when it was obtained in the same experiment with at least two biological replicates.

5. Conclusions

The results that are presented indicate that strigolactones may be involved in plant responses to many different abiotic stresses (flooding, wounding, cold) and biotic stresses (attack of viruses, bacteria, fungi or insects) that have not been linked to this group of hormones before. Additionally, strigolactone production can be regulated in many different ways since genes that are involved in this process are under the regulation of the TFs that are related to almost all classes of plant hormones. During the analysis of the genes in both species, it was possible to distinguish the group of TFs that is able to regulate the expression of all of the genes from individual species that were analyzed, as well as TFs that bind the promoters of all of the genes that have already been identified for Arabidopsis and rice. Additionally, the universal mechanism of the post-transcriptional regulation of gene activity via miRNAs was also present in both species. Taken together, these results indicate that up- or down-regulation of all of the components in the strigolactone biosynthesis pathway are necessary in some aspects of plant growth or adaptation to environmental stimuli. However, an even more important conclusion comes from the observation that each gene also has an individual mechanism for regulation that is related to TFs, as well as miRNAs. These observations are consistent with experimental data that has already been published and that indicate that the role of strigolactones in stress response or plant developmental program may be restricted only to the individual stages of their production.
We believe that data that is presented will facilitate the planning of future experiments that will allow our assumptions about the new roles of strigolactones in plants, especially those that are related to the responses to biotic stresses or metabolism that have not been postulated before, to be confirmed.

Acknowledgments

We would like to thank Barbara Wojcikowska and Anna Wojcik (Department of Genetics, University of Silesia) for the stimulating discussions during the preparation of the manuscript.
This research was supported by grants from the Foundation for Polish Science under the VENTURES program (2011-7/7) and was co-financed by the European Union, Regional Development Fund. Marek Marzec was supported by the Foundation for Polish Science scholarship (START 071/2014).

Author Contributions

Marek Marzec contributed to generation of the concept, interpretation of the data and writing of the manuscript; Aleksandra Muszynska contributed to interpretation of the data and writing of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Cook, C.E.; Whichard, L.P.; Turner, B.; Wall, M.E.; Egley, G.H. Germination of witchweed (Striga lutea Lour.): Isolation and properties of a potent stimulant. Science 1966, 154, 1189–1190. [Google Scholar] [CrossRef] [PubMed]
  2. Akiyama, K.; Matsuzaki, K.; Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 2005, 7043, 824–827. [Google Scholar] [CrossRef]
  3. Soto, M.J.; Fernandez-Aparicio, M.; Castellanos-Morales, V.; Garcia-Garrido, J.A.; Delgado, M.J.; Vierheilig, H. First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol. Biochem. 2010, 42, 383–385. [Google Scholar] [CrossRef]
  4. Gomez-Roldan, V.; Fermas, S.; Brewer, P.B.; Puech-Pagès, V.; Dun, E.A.; Pillot, J.P.; Letisse, F.; Matusova, R.; Danoun, S.; Portais, J.C.; et al. Strigolactone inhibition of shoot branching. Nature 2008, 455, 189–194. [Google Scholar] [CrossRef] [PubMed]
  5. Umehara, M.; Hanada, A.; Yoshida, S.; Akiyama, K.; Arite, T.; Takeda-Kamiya, N.; Magome, H.; Kamiya, Y.; Shirasu, K.; Yoneyama, K.; et al. Inhibition of shoot branching by new terpenoid plant hormones. Nature 2008, 455, 195–200. [Google Scholar] [CrossRef] [PubMed]
  6. Kapulnik, Y.; Delaux, P.M.; Resnick, N.; Mayzlish-Gati, E.; Wininger, S.; Bhattacharya, C.; Séjalon-Delmas, N.; Combier, J.P.; Bécard, G.; Belausov, E.; et al. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 2011, 233, 209–216. [Google Scholar] [CrossRef] [PubMed]
  7. Koltai, H. Strigolactones are regulators of root development. New Phytol. 2011, 190, 545–549. [Google Scholar] [CrossRef] [PubMed]
  8. Hu, Z.; Yan, H.; Yang, J.; Yamaguchi, S.; Maekawa, M.; Takamure, I.; Tsutsumi, N.; Kyozuka, J.; Nakazono, M. Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol. 2010, 51, 1136–1142. [Google Scholar] [CrossRef] [PubMed]
  9. De Saint Germain, A.; Ligerot, Y.; Dun, E.A.; Pillot, J.P.; Ross, J.J.; Beveridge, C.A.; Rameau, C. Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol. 2013, 163, 1012–1025. [Google Scholar] [CrossRef] [PubMed]
  10. Agusti, J.; Herold, S.; Schwarz, M.; Sanchez, P.; Ljung, K.; Dun, E.A.; Brewer, P.B.; Beveridge, C.A.; Sieberer, T.; Sehr, E.M.; et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl. Acad. Sci. USA 2011, 108, 20242–20247. [Google Scholar] [CrossRef] [PubMed]
  11. Sang, D.; Chen, D.; Liu, G.; Liang, Y.; Huang, L.; Meng, X.; Chu, J.; Sun, X.; Dong, G.; Yuan, Y.; et al. Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl. Acad. Sci. USA 2014, 111, 11199–11204. [Google Scholar] [CrossRef] [PubMed]
  12. Brewer, P.B.; Koltai, H.; Beveridge, C.A. Diverse roles of strigolactones in plant development. Mol. Plant 2013, 6, 18–28. [Google Scholar] [CrossRef] [PubMed]
  13. Kapulnik, Y.; Koltai, H. Strigolactone involvement in root development, response to abiotic stress and interactions with the biotic soil environment. Plant Physiol. 2014, 166, 560–569. [Google Scholar] [CrossRef] [PubMed]
  14. Waldie, T.; McCulloch, H.; Leyser, O. Strigolactones and the control of plant development: Lessons from shoot branching. Plant J. 2014, 79, 607–622. [Google Scholar] [CrossRef] [PubMed]
  15. Yoneyama, K.; Yoneyama, K.; Takeuchi, Y.; Sekimoto, H. Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 2007, 225, 1031–1038. [Google Scholar] [CrossRef] [PubMed]
  16. Yoneyama, K.; Xie, X.; Kisugi, T.; Nomura, T.; Yoneyama, K. Nitrogen and phosphorus fertilization negatively affects strigolactone production and exudation in sorghum. Planta 2013, 238, 885–894. [Google Scholar] [CrossRef] [PubMed]
  17. Yoneyama, K.; Xie, X.; Kusumoto, D.; Sekimoto, H.; Sugimoto, Y.; Takeuchi, Y.; Yoneyama, K. Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 2007, 227, 125–132. [Google Scholar] [CrossRef] [PubMed]
  18. Yoneyama, K.; Xie, X.; Kim, H.I.; Kisugi, T.; Nomura, T.; Sekimoto, H.; Yokota, T.; Yoneyama, K. How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 2012, 235, 1197–1207. [Google Scholar] [CrossRef] [PubMed]
  19. López-Ráez, J.A.; Charnikhova, T.; Gómez-Roldán, V.; Matusova, R.; Kohlen, W.; de Vos, R.; Verstappen, F.; Puech-Pages, V.; Bécard, G.; Mulder, P.; et al. Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol. 2008, 178, 863–874. [Google Scholar] [CrossRef] [PubMed]
  20. Foo, E.; Yoneyama, K.; Hugill, C.J.; Quittenden, L.J.; Reid, J.B. Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol. Plant 2013, 6, 76–87. [Google Scholar] [CrossRef] [PubMed]
  21. Marzec, M.; Muszynska, A.; Gruszka, D. The role of strigolactones in nutrient-stress responses in plants. Int. J. Mol. Sci. 2014, 14, 9286–9304. [Google Scholar] [CrossRef]
  22. Aroca, R.; Ruiz-Lozano, J.M.; Zamarreño, A.M.; Paz, J.A.; García-Mina, J.M.; Pozo, M.J.; López-Ráez, J.A. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 2013, 170, 47–55. [Google Scholar] [CrossRef] [PubMed]
  23. Bu, Q.; Lv, T.; Shen, H.; Luong, P.; Wang, J.; Wang, Z.; Huang, Z.; Xiao, L.; Engineer, C.; Kim, T.H.; et al. Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiol. 2014, 164, 424–439. [Google Scholar] [CrossRef] [PubMed]
  24. Ha, C.V.; Leyva-González, M.A.; Osakabe, Y.; Tran, U.T.; Nishiyama, R.; Watanabe, Y.; Tanaka, M.; Seki, M.; Yamaguchi, S.; Dong, N.V.; et al. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc. Natl. Acad. Sci. USA 2014, 111, 851–856. [Google Scholar] [CrossRef] [PubMed]
  25. Matusova, R.; Rani, K.; Verstappen, F.W.; Franssen, M.C.; Beale, M.H.; Bouwmeester, H.J. The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol. 2005, 139, 920–934. [Google Scholar] [CrossRef] [PubMed]
  26. Zwanenburg, B.; Mwakaboko, A.S.; Reizelman, A.; Anilkumar, G.; Sethumadhavan, D. Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Manag. Sci. 2009, 65, 478–491. [Google Scholar] [CrossRef] [PubMed]
  27. Xie, X.; Yoneyama, K.; Yoneyama, K. The strigolactone story. Ann. Rev. Phytopathol. 2010, 48, 93–117. [Google Scholar] [CrossRef]
  28. Xie, X.; Yoneyama, K.; Kisugi, T.; Uchida, K.; Ito, S.; Akiyama, K.; Hayashi, H.; Yokota, T.; Nomura, T.; Yoneyama, K. Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol. Plant 2013, 6, 153–163. [Google Scholar] [CrossRef] [PubMed]
  29. Alder, A.; Jamil, M.; Marzorati, M.; Bruno, M.; Vermathen, M.; Bigler, P.; Ghisla, S.; Bouwmeester, H.; Beyer, P.; Al-Babili, S. The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 2012, 335, 1348–1351. [Google Scholar] [CrossRef] [PubMed]
  30. Lin, H.; Wang, R.; Qian, Q.; Yan, M.; Meng, X.; Fu, Z.; Yan, C.; Jiang, B.; Su, Z.; Li, J.; et al. DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 2009, 21, 1512–1525. [Google Scholar] [CrossRef] [PubMed]
  31. Waters, M.T.; Brewer, P.B.; Bussell, J.D.; Smith, S.M.; Beveridge, C.A. The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiol. 2012, 159, 1073–1085. [Google Scholar] [CrossRef] [PubMed]
  32. Proust, H.; Hoffmann, B.; Xie, X.; Yoneyama, K.; Schaefer, D.G.; Yoneyama, K.; Nogué, F.; Rameau, C. Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 2011, 138, 1531–1539. [Google Scholar] [CrossRef] [PubMed]
  33. Wang, R.K.; Lu, J.J.; Xing, G.N.; Gai, J.Y.; Zhao, T.J. Molecular evolution of two consecutive carotenoid cleavage dioxygenase genes in strigolactone biosynthesis in plants. Genet. Mol. Res. 2011, 10, 3664–3673. [Google Scholar] [CrossRef] [PubMed]
  34. Booker, J.; Auldridge, M.; Wills, S.; McCarty, D.; Klee, H.; Leyser, O. MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr. Biol. 2004, 14, 1232–1238. [Google Scholar] [CrossRef] [PubMed]
  35. Ishikawa, S.; Maekawa, M.; Arite, T.; Onishi, K.; Takamure, I.; Kyozuka, J. Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 2005, 46, 79–86. [Google Scholar] [CrossRef] [PubMed]
  36. Zou, J.; Zhang, S.; Zhang, W.; Li, G.; Chen, Z.; Zhai, W.; Zhao, X.; Pan, X.; Xie, Q.; Zhu, L. The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J. 2006, 48, 687–698. [Google Scholar] [CrossRef] [PubMed]
  37. Beveridge, C.A.; Kyozuka, J. New genes in the strigolactone-related shoot branching pathway. Curr. Opin. Plant Biol. 2010, 13, 34–39. [Google Scholar] [CrossRef] [PubMed]
  38. Scaffidi, A.; Waters, M.T.; Ghisalberti, E.L.; Dixon, K.W.; Flematti, G.R.; Smith, S.M. Carlactone-independent seedling morphogenesis in Arabidopsis. Plant J. 2013, 76, 1–9. [Google Scholar] [PubMed]
  39. Seto, Y.; Sado, A.; Asami, K.; Hanada, A.; Umehara, M.; Akiyama, K.; Yamaguchi, S. Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc. Natl. Acad. Sci. USA 2014, 111, 1640–1645. [Google Scholar] [CrossRef] [PubMed]
  40. Booker, J.; Sieberer, T.; Wright, W.; Williamson, L.; Willett, B.; Stirnberg, P.; Turnbull, C.; Srinivasan, M.; Goddard, P.; Leyser, O. MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev. Cell 2005, 8, 443–449. [Google Scholar] [CrossRef] [PubMed]
  41. Cardoso, C.; Zhang, Y.; Jamil, M.; Hepworth, J.; Charnikhova, T.; Dimkpa, S.O.; Meharg, C.; Wright, M.H.; Liu, J.; Meng, X. Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc. Natl. Acad. Sci. USA 2014, 111, 2379–2384. [Google Scholar] [CrossRef] [PubMed]
  42. Zhang, Y.; van Dijk, A.D.; Scaffidi, A.; Flematti, G.R.; Hofmann, M.; Charnikhova, T.; Verstappen, F.; Hepworth, J.; van der Krol, S.; Leyser, O.; et al. Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat. Chem. Biol. 2014, 10, 1028–1033. [Google Scholar] [CrossRef] [PubMed]
  43. Abe, S.; Sado, A.; Tanaka, K.; Kisugi, T.; Asami, K.; Ota, S.; Kim, H.I.; Yoneyama, K.; Xie, X.; Ohnishi, T.; et al. Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc. Natl. Acad. Sci. USA 2014, 111, 18084–18089. [Google Scholar] [CrossRef] [PubMed]
  44. Xue, L.J.; Zhang, J.J.; Xue, H.W. Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res. 2009, 37, 916–930. [Google Scholar] [CrossRef] [PubMed]
  45. Winter, D.; Vinegar, B.; Nahal, H.; Ammar, R.; Wilson, G.V.; Provart, N.J. An “Electronic Fluorescent Pictograph” Browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2007, 2, e718. [Google Scholar] [CrossRef] [PubMed]
  46. Arabidopsis eFP Browser. Available online: http://bar.utoronto.ca/efp (accessed on 11–30 November 2014).
  47. Bolivar, J.C.; Machens, F.; Brill, Y.; Romanov, A.; Bülow, L.; Hehl, R. “In silico expression analysis”, a novel PathoPlant web tool to identify abiotic and biotic stress conditions associated with specific cis-regulatory sequences. Database 2014. [CrossRef]
  48. PathoPlant. Available online: http://www.pathoplant.de (accessed on 11–30 November 2014).
  49. Sato, Y.; Takehisa, H.; Kamatsuki, K.; Minami, H.; Namiki, N.; Ikawa, H.; Ohyanagi, H.; Sugimoto, K.; Antonio, B.A.; Nagamura, Y. RiceXPro version 3.0: Expanding the informatics resource for rice transcriptome. Nucleic Acids Res. 2013, 41, D1206–D1213. [Google Scholar] [CrossRef] [PubMed]
  50. RiceXPro. Available online: http://ricexpro.dna.affrc.go.jp (accessed on 15–30 November 2014).
  51. Kilian, J.; Whitehead, D.; Horak, J.; Wanke, D.; Weinl, S.; Batistic, O.; D’Angelo, C.; Bornberg-Bauer, E.; Kudla, J.; Harter, K. The AtGenExpress global stress expression data set: Protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 2007, 50, 347–363. [Google Scholar] [CrossRef] [PubMed]
  52. Ruyter-Spira, C.; Al-Babili, S.; van der Krol, S.; Bouwmeester, H. The biology of strigolactones. Trends Plant Sci. 2013, 18, 72–83. [Google Scholar] [CrossRef] [PubMed]
  53. Meshi, T.; Iwabuchi, M. Plant transcription factors. Plant Cell Physiol. 1995, 36, 1405–1420. [Google Scholar] [PubMed]
  54. Lan, A.; Huang, J.; Zhao, W.; Peng, Y.; Chen, Z.; Kang, D. A salicylic acid-induced rice (Oryza sativa L.) transcription factor OsWRKY77 is involved in disease resistance of Arabidopsis thaliana. Plant Biol. 2013, 15, 452–461. [Google Scholar] [CrossRef] [PubMed]
  55. Negi, J.; Moriwaki, K.; Konishi, M.; Yokoyama, R.; Nakano, T.; Kusumi, K.; Hashimoto-Sugimoto, M.; Schroeder, J.I.; Nishitani, K.; Yanagisawa, S.; et al. A Dof transcription factor, SCAP1, is essential for the development of functional stomata in Arabidopsis. Curr. Biol. 2013, 23, 479–484. [Google Scholar] [CrossRef] [PubMed]
  56. Herrero, J.; Esteban Carrasco, A.; Zapata, J.M. Arabidopsis thaliana peroxidases involved in lignin biosynthesis: In silico promoter analysis and hormonal regulation. Plant Physiol. Biochem. 2013, 80, 192–202. [Google Scholar] [CrossRef]
  57. Yadav, D.K.; Shukla, D.; Tuteja, N. Rice heterotrimeric G-protein alpha subunit (RGA1): In silico analysis of the gene and promoter and its upregulation under abiotic stress. Plant Physiol. Biochem. 2013, 63, 262–271. [Google Scholar] [CrossRef] [PubMed]
  58. Zhu, Q.L.; Xie, X.R.; Zhang, J.; Xiang, G.; Li, Y.; Wu, H.B. In silico analysis of a MRP transporter gene reveals its possible role in anthocyanins or flavonoids transport in Oryza sativa. Am. J. Plant Sci. 2013, 4, 555. [Google Scholar] [CrossRef]
  59. Jensen, M.K.; Lindemose, S.; Masi, F.D.; Reimer, J.J.; Nielsen, M.; Perera, V.; Workman, C.T.; Turck, F.; Grant, M.R.; Mundy, J.; et al. ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Biol. 2013, 3, 321–327. [Google Scholar] [CrossRef] [Green Version]
  60. Sakamoto, T.; Morinaka, Y.; Inukai, Y.; Kitano, H.; Fujioka, S. Auxin signal transcription factor regulates expression of the brassinosteroid receptor gene in rice. Plant J. 2013, 73, 676–688. [Google Scholar] [CrossRef] [PubMed]
  61. Sun, H.; Tao, J.; Liu, S.; Huang, S.; Chen, S.; Xie, X.; Yoneyama, K.; Zhang, Y.; Xu, G. Strigolactones are involved in phosphate-and nitrate-deficiency-induced root development and auxin transport in rice. J. Exp. Bot. 2014, 65, 6735–6746. [Google Scholar] [CrossRef] [PubMed]
  62. Djennane, S.; Hibrand-Saint Oyant, L.; Kawamura, K.; Lalanne, D.; Laffaire, M.; Thouroude, T.; Chalain, S.; Sakr, S.; Boumaza, R.; Foucher, F.; et al. Impacts of light and temperature on shoot branching gradient and expression of strigolactone synthesis and signalling genes in rose. Plant Cell Environ. 2014, 37, 742–757. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Cui, X. Strigolactones, karrikins and more: Newly discovered molecules light up plant signaling. Mol. Plant 2014, 7, 579–581. [Google Scholar] [CrossRef]
  64. Yu, D.; Chen, C.; Chen, Z. Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 2001, 13, 1527–1540. [Google Scholar] [CrossRef] [PubMed]
  65. Dong, J.; Chen, C.; Chen, Z. Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol. Biol. 2003, 51, 21–37. [Google Scholar] [CrossRef] [PubMed]
  66. Kalde, M.; Barth, M.; Somssich, I.E.; Lippok, B. Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol. Plant Microbe Interact. 2003, 16, 295–305. [Google Scholar] [CrossRef] [PubMed]
  67. Liu, X.; Bai, X.; Wang, X.; Chu, C. OsWRKY71, a rice transcription factor, is involved in rice defense response. J. Plant Physiol. 2007, 164, 969–979. [Google Scholar] [CrossRef] [PubMed]
  68. Gutha, L.R.; Reddy, A.R. Rice DREB1B promoter shows distinct stress-specific responses and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol. Biol. 2008, 68, 533–555. [Google Scholar] [CrossRef] [PubMed]
  69. Pozo, M.J.; Jung, S.C.; López-Ráez, J.A.; Azcón-Aguilar, C. Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: The role of plant defence mechanisms. In Arbuscular Mycorrhizas: Physiology and Function; Koltai, H., Kapulnik, Y., Eds.; Springer: Dordrecht, The Netherlands, 2010; pp. 193–207. [Google Scholar]
  70. Mohanty, B.; Krishnan, S.P.T.; Swarup, S.; Bajic, V.B. Detection and preliminary analysis of motifs in promoters of anaerobically induced genes of different plant species. Ann. Bot. 2005, 96, 669–681. [Google Scholar] [CrossRef] [PubMed]
  71. Zhang, J.; van Toai, T.; Huynh, L.; Preiszner, J. Development of flooding-tolerant Arabidopsis thaliana by autoregulated cytokinin production. Mol. Breed. 2000, 6, 135–144. [Google Scholar] [CrossRef]
  72. Zhai, L.; Liu, Z.; Zou, X.; Jiang, Y.; Qiu, F.; Zheng, Y.; Zhang, Z. Genome-wide identification and analysis of microRNA responding to long-term waterlogging in crown roots of maize seedlings. Physiol. Plant. 2013, 147, 181–193. [Google Scholar] [CrossRef] [PubMed]
  73. Jung, J.H.; Seo, P.J.; Park, C.M. MicroRNA biogenesis and function in higher plants. Plant Biotechnol. Rep. 2009, 3, 111–126. [Google Scholar] [CrossRef]
  74. Voinnet, O. Origin, biogenesis and activity of plant microRNAs. Cell 2009, 136, 669–687. [Google Scholar] [CrossRef] [PubMed]
  75. Si-Ammour, A.; Windels, D.; Arn-Bouldoires, E.; Kutter, C.; Ailhas, J.; Meins, F.; Vazquez, F. miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxin-related development of Arabidopsis leaves. Plant Physiol. 2009, 157, 683–691. [Google Scholar] [CrossRef]
  76. Ding, Y.; Tao, Y.; Zhu, C. Emerging roles of microRNAs in the mediation of drought stress response in plants. J. Exp. Bot. 2013, 64, 3077–3086. [Google Scholar] [CrossRef] [PubMed]
  77. Tang, S.; Wang, Y.; Li, Z.; Gui, Y.; Xiao, B.; Xie, J.; Zhu, Q.H.; Fan, L. Identification of wounding and topping responsive small RNAs in tobacco (Nicotiana tabacum). BMC Plant Biol. 2012, 12, 28. [Google Scholar] [CrossRef] [PubMed]
  78. Raghuram, B.; Sheikh, A.H.; Rustagi, Y.; Sinha, A.K. MicroRNA biogenesis factor DRB1 is a phosphorylation target of mitogen activated protein kinase, MPK3 in both rice and Arabidopsis. FEBS J. 2014, 282, 521–536. [Google Scholar] [CrossRef] [PubMed]
  79. Rhoades, M.W.; Reinhart, B.J.; Lim, L.P.; Burge, C.B.; Bartel, B.; Bartel, D.P. Prediction of plant microRNA targets. Cell 2002, 110, 513–520. [Google Scholar] [CrossRef] [PubMed]
  80. Cheng, X.; Ruyter-Spira, C.; Bouwmeester, H. The interaction between strigolactones and other plant hormones in the regulation of plant development. Front. Plant Sci. 2013, 4, 199. [Google Scholar] [CrossRef] [PubMed]
  81. Crawford, S.; Shinohara, N.; Sieberer, T.; Williamson, L.; George, G.; Hepworth, J.; Müller, D.; Domagalska, M.A.; Leyser, O. Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 2010, 137, 2905–2913. [Google Scholar] [CrossRef] [PubMed]
  82. Shinohara, N.; Taylor, C.; Leyser, O. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 2013, 11, e1001474. [Google Scholar] [CrossRef] [PubMed]
  83. Dun, E.A.; de Saint Germain, A.; Rameau, C.; Beveridge, C.A. Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol. 2012, 158, 487–498. [Google Scholar] [CrossRef] [PubMed]
  84. Hayward, A.; Stirnberg, P.; Beveridge, C.; Leyser, O. Interactions between auxin and strigolactone in shoot branching control. Plant Physiol. 2009, 151, 400–412. [Google Scholar] [CrossRef] [PubMed]
  85. Foo, E.; Bullier, E.; Goussot, M.; Foucher, F.; Rameau, C.; Beveridge, C.A. The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 2005, 17, 464–474. [Google Scholar] [CrossRef] [PubMed]
  86. Arite, T.; Iwata, H.; Ohshima, K.; Maekawa, M.; Nakajima, M.; Kojima, M.; Sakakibara, H.; Kyozuka, J. DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J. 2007, 51, 1019–1029. [Google Scholar] [CrossRef] [PubMed]
  87. Pandya-Kumar, N.; Shema, R.; Kumar, M.; Mayzlish-Gati, E.; Levy, D.; Zemach, H.; Belausov, E.; Wininger, S.; Abu-Abied, M.; Kapulnik, T.; et al. Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New Phytol. 2014, 202, 1184–1196. [Google Scholar] [CrossRef] [PubMed]
  88. Umehara, M.; Hanada, A.; Magome, H.; Takeda-Kamiya, N.; Yamaguchi, S. Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol. 2010, 51, 1118–1126. [Google Scholar] [CrossRef] [PubMed]
  89. Chang, W.C.; Lee, T.Y.; Huang, H.D.; Huang, H.Y.; Pan, R.L. PlantPAN: Plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC Genomics 2008, 9, 561. [Google Scholar] [CrossRef] [PubMed]
  90. Plant PAN. Available online: http://plantpan.mbc.nctu.edu.tw (accessed on 12–30 November 2014).
  91. Rice Annotation Project Database. Available online: http://rapdblegacy.dna.affrc.go.jp (accessed on 12–30 November 2014).
  92. Yilmaz, A.; Mejia-Guerra, M.K.; Kurz, K.; Liang, X.; Welch, L.; Grotewold, E. AGRIS: The arabidopsis gene regulatory information server, an update. Nucleic Acids Res. 2011, 39, D1118–D1122. [Google Scholar] [CrossRef] [PubMed]
  93. AGRIS. Available online: http://arabidopsis.med.ohio-state.edu (accessed on 15–30 November 2014).
  94. Mathelier, A.; Zhao, X.; Zhang, A.W.; Parcy, F.; Worsley-Hunt, R.; Arenillas, D.J.; Buchman, S.; Chen, C.Y.; Chou, A.; Ienasescu, H.; et al. JASPAR 2014: An extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 2014, 42, D142–D147. [Google Scholar] [CrossRef] [PubMed]
  95. YASPAR. Available online: http://jaspar.genereg.net (accessed on 15–30 November 2014).
  96. Higo, K.; Ugawa, Y.; Iwamoto, M.; Korenaga, T. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 1999, 27, 297–300. [Google Scholar] [CrossRef] [PubMed]
  97. PLACE. Available online: http://www.dna.affrc.go.jp/PLACE/ (accessed on 15–30 November 2014).
  98. Matys, V.; Fricke, E.; Geffers, R.; Gössling, E.; Haubrock, M.; Hehl, R.; Hornischer, K.; Karas, D.; Kel, A.E.; Kel-Margoulis, O.V.; et al. TRANSFAC: Transcriptional regulation, from patterns to profiles. Nucleic Acids Res. 2003, 31, 374–378. [Google Scholar] [CrossRef] [PubMed]
  99. TRANSFAC Database. Available online: http://www.gene-regulation.com/cgi-bin/pub/databases/transfac (accessed on 15–30 November 2014).
  100. Jin, J.P.; Zhang, H.; Kong, L.; Gao, G.; Luo, J.C. PlantTFDB 3.0: A portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. 2014, 42, D1182–D1187. [Google Scholar] [CrossRef] [PubMed]
  101. PlantTF Database. Available online: http://planttfdb.cbi.pku.edu.cn (accessed on 15–30 November 2014).
  102. Kozomara, A.; Griffiths-Jones, S. miRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 2014, 42, D68–D73. [Google Scholar] [CrossRef] [PubMed]
  103. miRBase. Available online: http://www.mirbase.org (accessed on 20–30 November 2014).

Share and Cite

MDPI and ACS Style

Marzec, M.; Muszynska, A. In Silico Analysis of the Genes Encoding Proteins that Are Involved in the Biosynthesis of the RMS/MAX/D Pathway Revealed New Roles of Strigolactones in Plants. Int. J. Mol. Sci. 2015, 16, 6757-6782. https://doi.org/10.3390/ijms16046757

AMA Style

Marzec M, Muszynska A. In Silico Analysis of the Genes Encoding Proteins that Are Involved in the Biosynthesis of the RMS/MAX/D Pathway Revealed New Roles of Strigolactones in Plants. International Journal of Molecular Sciences. 2015; 16(4):6757-6782. https://doi.org/10.3390/ijms16046757

Chicago/Turabian Style

Marzec, Marek, and Aleksandra Muszynska. 2015. "In Silico Analysis of the Genes Encoding Proteins that Are Involved in the Biosynthesis of the RMS/MAX/D Pathway Revealed New Roles of Strigolactones in Plants" International Journal of Molecular Sciences 16, no. 4: 6757-6782. https://doi.org/10.3390/ijms16046757

Article Metrics

Back to TopTop