PEBP/RKIPs interacting proteins.
The nature of Hd3a protein in rice and its ortholog FT in Arabidopsis as a florigen has been proposed. However, molecular mechanism of its function still remains to be investigated. Therefore, it is important to search their interaction partners to better understand their signaling in flowering. As a long-distance signal that moves along leaf cells and the vascular system of leaves and stem and exerts its action in apical buds, it is important to determine the possible mediators of such common responses activated by Hd3a. To search Hd3a interactor, yeast two-hybrid screening have performed by using a cDNA library. A wide range of Hd3a interacting proteins involved in signaling were identified, including GF14c, OsKANADI and the BRI1 kinase domain interacting protein 116b (BIP116b). To reveal its function, Hd3a recruits different protein in plant developmental stage. It is possible that Hd3a and its partner(s) may form a platform for cross-talk between signal transduction pathways. Another homolog of Hd3a in many plants was identified and sugessted that Hd3a/FT has versatile role in plant development. This role depend on its partner and interaction to achieve its function. Our understanding in floral transition in rice would make for better crop management in future.
- interacting proteins
Transition from vegetative phase to flowering involves many genetic pathways that interact with the external signals, such as day length and temperature, and internal signals such as hormones and developmental controls. One of the most important factors controlling flowering plants is response to daylight or photoperiod . Based on photoperiodism, two model plants,
Hd3a shares sequence similarity with the mammalian phosphatidylethanolamine-binding protein (PEBP or RAF1 kinase inhibitor protein—RKIP) (Figure 2). The PEBP family regulates signaling pathways to control growth and differentiation. The PEBPs seem to act biochemically as inhibitors, binding signaling components to modulate the flux through their pathways.
The crystal structure of PEBP from human and bovine sources, CEN protein from
PEBPs might also act as either scaffolds for or regulators of signaling complexes, as showed by the finding that Self-Pruning (SP) and Single-Flower Truss (SFT), as a tomato homolog of Terminal Flowering Locus 1 (TFL1) and Flowering Locus T (FT), respectively, can interact with a range of diverse proteins [10, 11]. Several studies of protein interactions involving FT/Hd3a orthologs have been published. In
|Self-Pruning (SP) tomato||14-3-3 (adapter protein)|
SPGB (a putative bZIP transcription factor)
SPAK (SP-associated kinase)
|Flowering Locus T (FT) ||FD (bZIP transcription factor)||[12, 13]|
|Single-Flower Truss (SFT) tomato||SPGB|
In this chapter, we will discuss the regulation of Hd3a florigen in rice and the identification of novel interaction partners for rice Hd3a protein using yeast two-hybrid screening. The interaction between Hd3a and its partners was further confirmed by several methods, such as yeast two-hybrid assay using full-length cDNA,
2. Flowering regulation in rice
In rice (
Several unique genes in rice were isolated.
During the vegetative phase in rice, the shoot apical meristem (SAM) produces a series of leaves. The vegetative parts of the rice plant, consisting of root, culm, and leaves, form a tiller. A dramatic change occurs during the transition from vegetative to reproductive stages, with the tiller terminating to produce leaf and the panicle (inflorescence) being generated on the uppermost internode of the culm (Figure 4). The development stage of the young panicle is also related to the timing of leaf emergence. The differentiation stage of the young panicle almost directly correlates with the start of emergence of the fourth leaf (counted downward from the flag leaf). At the time of flag leaf (small last leaf) emergence, the glumes flower primordial has already differentiated and pollen mother cells are being formed . The flag leaf, contributes largely to the filling of grains because it supplies photosynthetic products mainly to the panicle.
Flowering time in rice is indicated by the emergence of the flag leaf or the panicle (heading date). The panicle is initiated when the first bract primordium differentiates on the shoot apex, approximately 30 days before panicle emergence (heading). The start of differentiation of the glumes flower primordial follows after the rachis-branches differentiation has occurred (24 days before heading). The pistil and stamen differentiate 20 days before heading. Meiosis in the anther occurs 12 days before heading, and flower organ completion occurs 1–2 days before heading.
3. Yeast two-hybrid screening for searching Hd3a-interacting proteins
An important element in the characterization of Hd3a function is the identification of other proteins with which it interacts. To reveal the function of Hd3a in rice, yeast two-hybrid system was used as a tool for screening Hd3a-interacting proteins. This system consist of a fusion of protein interest to a DNA-binding domain (DBD-Hd3a) as a bait, and a fusion of cDNA library to a transcriptional activation domain (AD-cDNA library) as a prey (Figure 5). The DNA binding domain (DBD) recognizes a specific sequence in the DNA upstream of a promoter and the activation domain (AD) stimulates transcription by binding to RNA polymerase. If the two domains interact, they will activate transcription. In the two-hybrid system, both the DBD domain and the AD domain are fused to two other proteins. If the bait captures the prey, means that proteins are interacting, a complex will be formed and the reporter gene will be activated. The reporter gene is used to monitor for a successful interaction.
As a tool for searching Hd3a interactors, the construction of a bait and prey is important. cDNA library were constructed from leaf blades harvested 35 days after sowing at ZT 0, 2, and 4 when transition from vegetative to reproductive phase occurred and
For the large-scale yeast two-hybrid screen, a total of ~1.6 × 106 transformants were screened for activation of histidine synthase 3 (HIS3) onto selective medium plates without amino acids leucine (L), tryptophan (W) and histidine (SC-His). In the first screening on media SC-His, 354 colonies were obtained. The next screening on medium SC-His containing 3-AT, a total of 96 colonies’ unique proteins were identified as positive clones. To eliminate false positive, we used 2.5 mM 3-AT, a competitive inhibitor of the
|Homologous proteins||Accession number||Two-hybrid*||Amino acids**||Domain/Function|
|Ribulose 1,5-biphosphate carboxilase (RuBisCO) small subunit||gi|3063524||150||175||RuBisCO|
|RuBisCO activase large isoform precursor protein||gi|77552725||162||466||RuBisCO|
|Putative RNA helicase||gi|34897325||127||756||–|
|Putative 40S ribosomal protein||gi|50939279||211||305||–|
|Translation initiation factor 5A/eIF5A||gi|50918889||161||161||–|
|Beta cyanoalanine synthase||gi|55233175||377||377||–|
|Putative anthranilate phosphoribosyltransferase||gi|50905035||121||141||–|
|Putative NADPH-dependent retinol dehydrogenase/reductase||gi|50726535||170||253||–|
|Putative SF16 protein||gi|50931997||240||500||–|
|Putative heat shock 70 KD protein (HSP70)||gi|27476086||157||657||chaperone|
|Putative glutathione S-transferase||gi|50900303||142||223||–|
|Thioredoxin H-type (TRX-H)||gi|50934769||204||350||–|
The main group of proteins identified in this yeast two-hybrid screen belongs to the class of signal transduction pathway components (57%). Others are classified as proteins that are involved in carbohydrate metabolism, protein/RNA/DNA synthesis, and proteins with unknown function. Interestingly, our yeast two-hybrid screening identified a diverse range of proteins that are mainly involved in signaling. In this chapter, we focus on three candidates: (i) GF14c (G box factor 14c), a 14-3-3 protein identified as a protein that is involved in signaling pathway. The recent results revealed that Ha3a, 14-3-3 and FD form a hexameric florigen activation complex (FAC) and in shoot apical meristem cells, 14-3-3 protein act as intracellular receptor for florigen ; (ii) BRI1-kinase domain (KD)-interacting protein 116b, and (iii) a novel myb transcription factor-like protein, namely OsKANADI1.
4. Rice flowering regulation by Hd3a and GF14c interaction
14-3-3 proteins in general bind to phosphoserine-modified proteins, as well as to some nonphosphorylated proteins such as exoenzyme S, which has no phosphorylated residue in its binding motif. They regulate the activities of a wide array of targets via direct protein-protein interactions, and effect changes in the client proteins. These changes can vary from inactivation or activation of the enzymatic activity of a target protein, to degradation or protection from degradation of the target, to movement of the target from one cellular location to another (usually nuclear-cytoplasmic shuttling). Plant 14-3-3 proteins bind a range of TFs and other signaling proteins, and have pivotal roles in regulating developmental and stress responses.
To reveal the biological functions of 14-3-3 in plants, the common approaches of generating overexpression, RNA suppression, or knockout plant lines probably have limited potential, for two reasons. First, because they interact with so many different targets, multiple pleiotropic effects would be expected. Second, 14-3-3s are encoded by a gene family with at least 12 expressed members in
Several studies of protein interactions involving FT/Hd3a orthologs have been published. In
4.1. Subcellular localization of Hd3a and GF14c
To identify the intracellular localization of Hd3a and GF14c, a fusion construct to express mCherry fluorescent protein-linked Hd3a under the ubiquitin promoter, and GFP-linked GF14c driven by the CaMV 35S promoter were made. These constructs were introduced into rice protoplasts. In all of the rice protoplasts observed in this experiment, Hd3a-mCherry localized in both cytoplasm and nucleus; however, GF14c-GFP was predominantly visualized in the cytoplasm (75% of rice protoplasts observed) (Figure 8). The predominant cytoplasmic localization of 14-3-3 proteins has led to the hypothesis that they might act as cytoplasmic anchors that either block import into the nucleus or other organelles, or promote export from organelles into the cytoplasm .
In vitro and in vivo interaction of Hd3a and GF14c
The interaction between Hd3a and GF14c was confirmed using several methods, including a GST pull-down assay, yeast two-hybrid and a co-immunoprecipitation . A GST-Hd3a fusion protein was pulled down with His-tagged GF14c, indicating that Hd3a interacted with GF14c
4.3. Bimolecular fluorescence complementation (BiFC) of Hd3a and GF14c
To determine the distribution of Hd3a and GF14c
4.4. Confirmation of Hd3a interacting protein GF14c by mutant generation
Several methods has been used to confirm the interaction between Hd3a and GF14c. All the methods used (yeast-two hybrid, in vitro pull-down, and BiFC assays) clearly showed that Hd3a and GF14c have strong interaction in rice. The subcellular distribution of Hd3a as well as GF14c demonstrated their localization in both the cytoplasm and nucleus.
GF14c acts as negative regulator of flowering and the overexpression of GF14c caused late flowering phenotype. Since the expression of Hd3a was observed both in the cytoplasm and nucleus, whereas GF14c is mainly in the cytoplasm, the possible interaction of these two protein is interesting to study. The mechanism of interaction of which GF14c would inhibit shuttling of Hd3a from the cytoplasm into the nucleus were confirmed by BiFC experiment. Based on data obtained it is clearly showed that Hd3a-GF14c is localized in cytoplasm. This indicate Hd3a-GF14c interaction lead to Hd3a cyoplasmic retention. The increasing of cytoplasmic retention of Hd3a can be explained as a model of late flowering by overexpression of GF14c. An example in
Another possible mechanism which can be explain the phenotype of GF14c overexpression and knockout mutant lines is the interaction between GF14c and Hd3a inhibit the movement of Hd3a from leaf to SAM. When GF14c expression level is low, Hd3a protein is capable to move along the floem to the SAM, since HD3a is small protein (about 20kDa) that is below of the size limit of plasmodesmata [37, 38]. The
According to Taoka  finding, 14-3-3 protein acts as intercellular receptor for Hd3a in the shoot apical cells. When Hd3a protein is transported to SAM, it will interact with 14-3-3 and form florigen activation complex (FAC). This FAC complex will be translocated into nucleus and binds to
5. Hd3a interaction with BIP116b and OsKANADI
Analysis of Hd3a interacting proteins in yeast two-hybrid screening identified a novel protein homolog of BIP116 (brassinosteroid-insensitive 1 [BRI1] kinase domain interacting protein 116) and a novel putative transcription factor belonging to the KANADI domain protein family, namely OsKANADI1 (OsKAN1).
5.1. Hd3a interact with BIP116b
BRI1 has an extracellular domain (containing an N-terminal signal peptide, and LRR-RK and island domains), a transmembrane domain, a kinase domain and a C-terminal peptide . Only a partial C-terminal region fragment was identified initially from yeast two-hybrid screening. An experiment using full-length Hd3a and full-length BIP116b, either as bait or as prey, further confirmed that Hd3a and BIP116b interact in the yeast system. To further study the interaction between Hd3a and BIP116b
The transgenic plant for either overexpression or RNAi mutant were generated. The results showed that the BIP116ab RNAi plants exhibited delayed flowering compared to wild-type plant, and the overexpressed plant showed branching and increasing tiller number similar to Hd3a overexpressed plants. Therefore, further characterization in mutant plants will be interesting to get an insight into its function.
5.2. Hd3a interact with OsKANADI1
Sequence analysis showed that OsKAN1 consists of six exons. Phylogenetic and comparative genetic analysis indicated that OsKAN1 is an ortholog of AtKANs and is most closely related to AtKAN4. The predicted OsKAN1 polypeptide contains a potential phosphorylation site in the C-terminal region which may be important for interaction with other proteins involved in signaling. The overall identity between
Suppression of OsKANADI1 by RNAi displayed branching and increasing tiller number in several lines . This phenotype resembles to the Hd3a overexpressed plants indicating that they possibly function in similar pathway. Further characterization using the OsKANADI mutants plants in the next generation remains to be investigated.
6. Hd3a homolog in plant development
The role of Hd3a as flowering mobile signal in rice and
The flowering and tuberization pathway are regulated in different pathways, indicating that FT has many homolog in potato. This hypothesis was confirmed by Navarro et al. . In potato, there are three homolog of FT. StSP3A regulate the tuber formation, StSP3D regulate the flowering, and StSP5G as the repressor of tuberization. Expression of
Recent study in onion tuberization reveals that its induction is controlled by Hd3a/FT homolog in the photoperiodic pathway. Onion is a biennial plant that forms tuber during the summer and flower after the winter in the next summer. There are many Hd3a/FT homologs found in onion and the pattern is the same with potato. There are Hd3a/FT homologs that regulate the tuber/bulb formation (AcFT1 and AcFT4) and flowering (AcFT2) . As seen in potato tuberization, AcFT4 in onion has the same role as StSP5G in potato that inhibits onion tuber formation; while AcFT1 is a strong inducer for tuberization (tuberigen) under long-day condition. This finding suggests that Hd3a/FT has a versatile role in plant development.
Tuberigen and florigen are known to be mobile/graft-transmissible signals. Several experiments showed that this signal is interchangeable between species in Solanaceae family (potato/tobacco, and potato/tomato) and can induce tuberization of potato and onion, but cannot in other plant species. As example, the ability to form a tuber is limited in potato species among Solanaceae family. Due to those fact, there must be an unknown mechanism present in the tuberization process in potato. The underlying mechanism that involves FT roles needs further investigation.
Another Hd3a role in rice as mobile signal that induced branching was reported by Tsuji et al. . Their findings suggest that Hd3a was moved along the xylem to promote branching in rice lateral meristem. The formation of florigen activation complex (FAC) for the developmental process other than flowering is not well understood. The experiment proved that Hd3a protein was transported to lateral meristem in the lateral bud and its transport is required for branching. This finding suggests that Hd3a has the function besides flowering.
Our work in local black rice namely “Cempo Ireng” which has very long harvest period also reveal that Hd3a gene is conserved. The regulation of flowering pathway of rice in short- and long-day condition is well understood. However, when rice are planted in neutral day condition such as tropical condition, the photoperiodic pathway might be affected. Our result suggests that Hd3a, which normally regulate flowering under short-day condition, is expressed in neutral day condition earlier compared to its homolog RFT1, which is responsible for flowering induction in long-day condition. In “Cempo Ireng,” two flowering genes are expressed. The expression pattern of both genes are redundant to induce the flowering under neutral day condition. RFT1 and Hd3a are known to have different induction pathways. Our result suggests that RFT1 and Hd3a may have independent pathway in rice flowering regulation under neutral day condition according to their expression pattern (data not shown). The Hd3a/RFT1 interactor of black rice that involved in flowering induction is of interest for future study to understand the flowering mechanism under neutral day condition and shortening the harvest period of black rice “Cempo Ireng.”
7. Conclusion and future prospects
As the floral stimulus that controls floral transition in the SAM, Hd3a has the capacity to traffic from cell to cell and move long distances via the phloem. To reveal its function, Hd3a recruits different proteins in plant developmental stage. A wide range of proteins that interact with Hd3a were identified using yeast two-hybrid screening. GF14c (a 14-3-3 homolog), OsKANADI (a novel transcription factor containing a GARP domain), and the BRI1 kinase domain-interacting protein 116b (BIP116b) are the Hd3a interactors of interest. It is possible that Hd3a and its partner(s) may form a platform for cross-talk between signal transduction pathways. Another homolog of Hd3a in many plants was identified and it was suggested that Hd3a/FT has versatile role in plant development. This role depends on its partner and interaction to gain its function. Further study using reverse genetics to obtain mutants, either gain-of-function mutants or suppression mutants by RNA interference of Hd3a partners to get insight into the function in plant growth and development, particularly during floral transition is important. Our understanding in floral transition in rice would make for better crop management in future and represent an important addition to our knowledge about FT signaling in plants.
This work was partially supported by The Ministry of Research, Technology and Higher education of Republic of Indonesia under the University Priority Research Program 2016 to YAP. We thank Badan Penerbit dan Publikasi Universitas Gadjah Mada (BPP UGM) for supporting this publication.
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