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General scheme of ethylene-induced biochemical pathways in latex cells. Factors in red and green are activated and inhibited by ethephon or ethylene, respectively. Factors are: Chi (Chitinase), Glu (Glucanase), GS (Glutamine synthetase), HEV (Hevein), HMG (3-hydroxy-3methylglutaryl-coenzyme A reductase), HXT (Hexose transporter), PIP (Plasma membrane intrinsic protein), RBOH (NADPH oxidase), REF (Rubber elongating factor), SUS (Sucrose synthase), SUT (Sucrose transporter). doi:10.1371/journal.pone.0099367.g001
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The AP2/ERF superfamily encodes transcription factors that play a key role in plant development and responses to abiotic and biotic stress. In Hevea brasiliensis, ERF genes have been identified by RNA sequencing. This study set out to validate the number of HbERF genes, and identify ERF genes involved in the regulation of latex cell metabolism. A c...
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... an ethylene releaser, is applied to the surface of the tapping panel to stimulate latex production. Ethephon induces several biochemical processes in laticifers [13], such as sucrose loading, water uptake, nitrogen assimilation or synthesis of defence proteins, involving a large number of ethylene-response genes [14][15][16][17][18][19][20], whereas its direct role in rubber biosynthesis is controversial [21] (Figure 1). For that reason, ethylene biosynthesis and signalling pathways have been intensively studied in Hevea [14,15,17,[22][23][24]. ...
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... members of this group were identified as key regulators of hypoxia-responsive genes in Arabidopsis but also in Oryza species. For that reason, an additional phylogenetic analysis was carried out using the 6 Hevea members, and 15 Oryza sativa and 2 Oryza nivara protein sequences, which have specific functions related to the response to submergence ( Figure S11 in File S1). This phylogenetic analysis showed that the HbERF-VIIa07 and HbERF-VIIa12 genes were found to be orthologs to the OsEREBP1. ...
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... previously demonstrated, transient transformation of protoplasts is a powerful tool for analysing the activity of transcription factors [47,50]. The GFP reporter gene under the control of a synthetic promoter harbouring the GCC box cis-acting element was transactivated by the three HbERF-VII candidates ( Figure 10). The effector constructs and the reporter constructs driven either by a GCC-rich synthetic promoter (GCC) or a synthetic promoter containing a mutated GCC motif (mGCC::TCCTCC) were co-transformed with 35S::HbERF-VII constructs into BY2 tobacco protoplasts. ...
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... rice has a larger number (15) of genes [6]. Interestingly, phylogenetic analysis of ERF group VII proteins revealed that Oryza sativa had one additional clade with Figure 10. Transactivation of the synthetic GCC-box and mGCC containing promoters by HbERF-VIIa7, HbERF-VIIa17 and HbERF- VIIa20 proteins. ...
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... S1 Contains Figure S1, Phylogenetic tree of ERF group I. The deduced amino acid sequences of the AP2 domain from Hevea (black letter) and Arabidopsis (blue letter) were aligned using Muscle, and the phylogenetic tree was constructed using PhyML with an LG+T model. ...
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... marker genes are indicated in bold letters. Figure S10, Phylogenetic tree of ERF group X. The deduced amino acid sequences of the AP2 domain from Hevea (black letter) and Arabidopsis (blue letter) were aligned using Muscle, and the phylogenetic tree was constructed using PhyML with an LG+T model. ...
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... marker genes are indicated in bold letters. Figure S11, Phylogenetic analysis of ERF group VII using the 6 Hevea brasiliensis, 15 Oryza sativa and 2 Oryza nivara members. The deduced amino acid sequences of the AP2 domain from Hevea (black letter) and Oryza sativa and Oryza nivara (green letter) were aligned using Muscle, and the phylogenetic tree was constructed using PhyML with an LG+T model. ...
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... Hal lain yang perlu menjadi perhatian saat ini selain pemupukan yaitu kegiatan penyadapan. Seringkali ditemui perusahaan perkebunan karet atau petani karet rakyat menerapkan penyadapan intensitas tinggi untuk memperoleh produksi maksimal namun berdampak negatif terhadap tanaman karet (Piyatrakul et al., 2014). Hasil penelitian (Junaidi et al., 2022;Kouadio et al., 2021) menyatakan bahwa tanaman karet yang disadap dengan intensitas tinggi akan berdampak terhadap persentase kering alur sadap (KAS) yang tinggi. ...
Fluctuating rubber prices cause rubber planters to suffer losses, especially when prices are low as of right now. Planters apply high-intensity tapping to obtain maximum production but this is not balanced with optimal fertilization and actually has a negative impact on the sustainability of rubber plantations. The purpose of this study was to determine the effect of a combination of fertilizing doses and tapping frequency on the productivity of rubber plants and to obtain optimal fertilizer doses and tapping frequency when rubber prices are low. The research method used a randomized block design (RBD), with six combination treatments of tapping frequency and fertilization. The results showed that the highest volume of latex was produced in the S/2 d3 ET treatment of 2.5% 100% fertilization, while the variable dry rubber content (DRC), tapping frequency treatment d3 (B, D, F) produced higher DRC and was significantly different compared to tapping frequency treatment d2 (A, C, E). The highest KKK was obtained in treatment F, namely 38.6%. Observation of individual plant production (g per tree per tapping), 50% - 100% fertilization treatment can increase the production of both tapping frequency d2 and d3. The highest production was obtained in treatment F (S/2 d3 ET2.5% 100% fertilization). So, tapping with d3 tapping frequency combined with 100% fertilization dose produces the highest individual plant productivity. Tapping with d3 frequency combined with 50% fertilization can be an alternative when the rubber price is low.
... pMDC107-GCC or pMDC107-mGCC, were constructed previously (Piyatrakul et al. 2014). The vectors of pMDC107-GCC or pMDC107-mGCC and HbERF expression vectors were co-transformed into tobacco protoplasts for transactivation activity detection. ...
... clade of ERF family with 8 AtERFs (Figure 1). A BLAST search against a comprehensive Hevea AP2/ERF superfamily database of 114 genes (Piyatrakul et al. 2014) revealed that three of the five HbERF genes had more than 98% nucleotide identities, respectively, with HbERF-IXc4, HbERF-IXa2 and HbERF-IXa3 in the database, whereas the two remaining had homologues of less than 80% sequence identity. (Table S5, Figure S2), justifying the obtaining of five HbERFs in our yeast one-hybrid screening with the HbSUT3 promoter as a bait (Table 1). ...
... (pMDC32-HbERF+GCC) ∕(pMDC32-HbERF+mGCC) − (pMDC32+GCC) ∕(pMDC32+mGCC) (Piyatrakul et al. 2014). Of the five HbERFs, four (HbERF-IXa2, HbERF-IXa3, HbERF-IXc4 and HbERF-IXc8) showed obvious transactivation activity, with HbERF-IXc4 being the strongest ( Figure 3B, Table S7). ...
Natural rubber is an important industrial raw material and commercially produced by rubber tree (Hevea brasiliensis). The sucrose transporter HbSUT3 plays an essential role in rubber production. Its expression in latex (cytoplasm of rubber-producing laticifers) is induced by bark treatment with Ethrel, an ethylene releaser, and the inducing effect correlates well with Ethrel-stimulated rubber yield increase. However, the mechanisms of ethylene induction on HbSUT3 expression are not known. Here, five Ethylene Response Factor (ERF) genes were identified from the cDNA library of Hevea latex by yeast one-hybrid screening with the promoter of HbSUT3 gene as bait. As revealed in a tobacco protoplast transient expression system, these HbERFs were mainly localized in the nucleus and four of them exhibited apparent transactivation activity. Of the five HbERF genes, HbERF-IXc4 was the most frequently screened in yeast one-hybrid, accounting for 65% of the ERF clones obtained. Moreover, among the five HbERFs, HbERF-IXc4 showed the strongest transactivation capacity when expressed in tobacco protoplast, the highest transcript abundance in latex, and a close expressional correlation with its target gene, HbSUT3, in response to the Ethrel treatment. Taken together, our results indicate that ERFs, especially HbERF-IXc4 is critically involved in the activation of HbSUT3 expression in latex after the Ethrel treatment on Hevea bark, and thus the stimulated latex yield.
... In this study, AP2/ERF family genes were identified in the Reyan 7-33-97 genome by detecting at least one AP2/ERF domain with 60 to 70 amino acids (pfam domain ID PF00847). There are three subfamilies in the AP2/ERF super family (Nakano et al. 2006;Piyatrakul et al. 2014 ...
The Hevea brasiliensis rubber tree is an important industrial crop that is widely planted in the tropical regions. China has a rubber planting history of more than 100 years and has successfully established three planting districts: Yunnan, Guangdong, and Hainan. More than 100 clones raised by Chinese breeders are widely cultivated. However, it is increasingly more difficult to raise yield through the conventional breeding approach due to the narrow genetic pool of Wickham germplasm and the low quality of genome assemblies of the rubber tree. With rapid advances in sequencing technology, it is now more convenient to sequence the genome of non-model plant species. The rubber tree genome is huge in size and high in heterozygosity, thus making genome assembly more challenging. To date, four versions of genomes have been published for the rubber tree, thus providing deep insights into genome structure and composition, species adaptation, rubber biosynthesis, and many agronomic traits. In this chapter, we describe the Reyan 7-33-97 genome and the gene families identified in it.
... Next generation sequencing technology accelerates the gene cloning and characterization in H. brasiliensis [29]. RNA-seq and in silico analysis have made a much important progress in identification of ethylene responsive transcriptional factors family AP2/ERF in H. brasiliensis [30,31]. However, ethylene signaling pathway involved in latex biosynthesis and drainage in H. brasiliensis still requires elucidation. ...
... EIN3/EILs are key transcriptional factors in ET signaling pathway. Activation of EIN3 and EILs by ET leads to EIN3/EILs-dependent transcriptional cascade [58,59], including hundreds of ethylene-regulated genes, such as AP2/ERF superfamily, which has been globally identified in H. brasiliensis [30,31]. Identification of HbEIN3/EILs is a key step to reveal the ET regulation pathway in H. brasiliensis. ...
EIN3/EILs are key regulators in ET signaling pathway. In this work, 4 members of EIN3/EILs of Hevea brasiliensis (HbEIN3/EILs) showed interaction with two F box proteins, HbEBF1 and HbEBF2. HbEIN3 located in nucleus and exhibited strong transcriptional activity. HbEIN3 was induced by ET treatment in C-serum, but not in B-serum of latex. HbEIN3/EILs bound to G-box cis-element. To globally search the potential targets of HbEIN3/EILs, genomic sequences of H. brasiliensis was re-annotated and an HCES (Hevea Cis-Elements Scanning) program was developed (www.h-brasiliensis.com). HCES scanning results showed that ET- and JA- responsive cis-elements distribute overlapping in gene promoters. 3146 genes containing G-box in promoters are potential targets of HbEIN3, including 41 genes involved in biosynthesis and drainage of latex, of which 7 rate-limiting genes of latex production were regulated by both ET and JA, suggesting that ET and JA signaling pathways coordinated the latex biosynthesis and drainage in H. brasiliensis.
Abbreviations: ABRE: ABA responsive elements; bHLH: basic helix-loop-helix; COG: Orthologous Groups; DRE: dehydration response element; ERE: ethylene responsive element; ET: Ethylene; GO: Gene Ontology; HCES: Hevea Cis-Elements Scanning; JA: jasmonates; JRE: Jasmonate-responsive element; KEGG: Kyoto Encyclopedia of Genes and Genomes; NR: non-redundant database; PLACE: Plant Cis-acting Regulatory DNA Elements; qRT-PCR: quantitative real-time RT-PCR.
... The AP2/ERF super family is one of the largest groups of transcription factors in plants. It includes all genes coding for at least one APETALA2 (AP2) domain and can be further separated into the ETHYLENE RESPONSE FACTOR (ERF), the AP2, and the RAV families (Piyatrakul et al., 2014). The RAV family encodes proteins possessing a single AP2 domain plus an additional B3 domain, which is also present in other, non-ERF transcription factors The AP2/ERF super family encodes transcription factors that play a key role in plant development and responses to abiotic and biotic stress. ...
... Seven of the 35 ERF expression marker genes were highly expressed in latex. Sub-cellular localization and transactivation analyses suggested that HbERF-VII candidate genes encoded functional transcription factors (Piyatrakul et al., 2014). ...
The commercial production of high quality natural rubber (NR) solely depends on Hevea brasiliensis Muell. Arg, (Para rubber tree) and accounts for >98% of total production worldwide. NR with its unique properties is an essential commodity for the automobile industry and its synthetic counterparts are in no way substitute to it. The rubber tree genome is very complex and plays an important role in delivering the unique properties of Hevea. But a lack of knowledge on the molecular mechanisms of rubber biosynthesis, disease resistance, etc., in elite clones of rubber still persists. Marker-assisted selection and transgenic techniques were proved to be advantageous in improving the breeding efficiency for latex yield, disease resistance, etc. The suppression subtractive hybridization (SSH), in the form of subtracted cDNA libraries and microarrays, can assist in searching the functions of expressed genes (candidate gene approach). Expressed sequence tags (ESTs) related to various metabolic aspects are well utilized to create EST banks that broadly represent the genes expressed in one tissue, such as latex cells, that assists in the study of gene function and regulation. Transcriptome analysis and gene mapping have been accomplished in Hevea at various stages. However, a selection criterion to delineate high yielding genotypes at the juvenile stage has not been accomplished so far. This is the main pit fall for rubber breeding apart from stock–scion interactions leading to yield differences among a clonally multiplied population. At least four draft genome sequences have been published on Hevea rubber, and all give different genome size and contig lengths—a comprehensive and acceptable genomic map remains unfulfilled. The progress made in molecular markers, latex biosynthesis genes, transcriptome analysis, chloroplast and mitochondrial DNA diversity, paternity identification through Breeding without Breeding (BwB), stimulated latex production and its molecular intricacies, molecular biology of tapping panel dryness, genomics for changed climates and genome mapping are discussed in this review. These information can be utilized to improvise the molecular breeding programs of Hevea in future.
... Data 2). Trimmed reads were mapped on the rubber clone PB 260 reference transcriptome 21 . Of the 86,941 contigs, 72,910 were previously annotated by BLASTX. ...
... Data 4) and 4 genes in clone Reyan7-33-97 23 . The reference genome has 181 Ethylene Response DEGs encoding ERF were identified in latex by Piyatrakul and co-workers 21 and in the present study, respectively. In clone Reyan7-33-97, 21 DEGs were reported 23 . ...
... These results suggest a regulation of ethylene responsive genes in latex by ERFs in these rubber clones. Several members of three ERF groups (I, VII, VIII) are highly expressed in latex 21 . HbERF-II and HbERF-VIIIa deduced proteins contained the repressor EAR motif. ...
Tapping Panel Dryness (TPD) affects latex production in Hevea brasiliensis. This physiological syndrome involves the agglutination of rubber particles, which leads to partial or complete cessation of latex flow. Latex harvesting consists in tapping soft bark. Ethephon can be applied to stimulate latex flow and its regeneration in laticifers. Several studies have reported transcriptome changes in bark tissues. This study is the first report on deep RNA sequencing of latex to compare the effect of ethephon stimulation and TPD severity. Trees were carefully selected for paired-end sequencing using an Illumina HiSeq 2000. In all, 43 to 60 million reads were sequenced for each treatment in three biological replicates (slight TPD trees without ethephon stimulation, and slight and severe TPD trees with ethephon treatment). Differentially expressed genes were identified and annotated, giving 8,111 and 728 in response to ethephon in slight TPD trees and in ethephon-induced severe TPD trees, respectively. A biological network of responses to ethephon and TPD highlighted the major influence of metabolic processes and the response to stimulus, especially wounding and jasmonate depression in TPD-affected trees induced by ethephon stimulation.
... The authors followed the MIQE guidelines (Bustin et al., 2010;Bustin et al., 2009;Udvardi et al., 2008). Real-time RT-PCR analysis was carried out using a Light Cycler 480 (Roche, Basel, Switzerland) as described in Piyatrakul et al., 2014;Putranto et al., 2015). The HbRH2b reference gene and the target genes were amplified in parallel allowing calculation of the relative gene expression ratio taking into account primer efficiencies (EcGSH1 primer pair: E = 1.89, ...
Oxidative stress occurring during in-vitro culture is detrimental for clonal propagation by somatic embryogenesis in particular in Hevea brasiliensis. In previous work, overexpression of the gene encoding the cytosolic reactive oxygen species detoxification enzyme HbCuZnSOD led to reduce somatic embryo regeneration in Hevea. In this study, the role of antioxidant was tested by overexpression of the E.coli GSH1 gene involved in glutathione biosynthesis in rubber embryogenic callus lines. Transgenic lines were successfully established and some plants were regenerated. Overexpression of EcGSH1 gene led to glutathione over-accumulation, and affected dramatically the somatic embryogenesis process and plant development. Upon a water deficit treatment, these plants displayed the greatest drop in photosynthetic nitrogen use efficiency, higher proline content, and higher glutathione reductase activity. Changes induced in transgenic lines overexpressing HbCuZnSOD and EcGSH1 were discussed as well as possible applications on plant material propagation, overcoming loss of natural rubber production through Tapping Panel Dryness, and tropical soil remediation.
... These sequences were used as a comparator for the identification of COBRA gene family in H. brasiliensis. As a model plant in molecular biology, the genome database of A. thaliana has full annotation and demonstrated functions ( Piyatrakul et al., 2014;Putranto et al., 2015a). An NCBI MEGA-BLAST + tblastn of A. thaliana COBRA gene family against H. brasiliensis genomic scaffolds was carried out using Galaxy ( Cock et al., 2015). ...
In this paper, the H. brasiliensis COBRA gene family, alleged to be involved in laticifer differentiation, was identified from the public rubber tree genome of Reyan 7-33-97 clone. A comparative analysis was carried out against A. thaliana genomic database. This analysis has resulted to the in silico validation of thirteen putative genes encoding glycophosphatidylinositol anchors (GPI) proteins harbored by nine Hevea genomic scaffolds. The sequence’s similarity of HbCOBL against AtCOBL genes were ranged from the threshold 50 to 81.58% covering 151 to 458 amino acid residues, respectively. Three partial and ten full-length protein sequences of HbCOBL genes were annotated. The partial protein sequences ranged from 89 to 184 amino acid residues as opposed to the full-length proteins ranging from 160 to 471 amino acid residues. Two types of COBRA domains (pfam04833 and cl04787) were found among HbCOBL genes. Phylogenetic analysis has clustered two subfamilies. Nine HbCOBL genes (HbCOBL-B, HbCOBL-J, HbCOBL-C, HbCOBL-H, HbCOBL-F, HbCOBL-I, HbCOBL-M, HBCOBL-A, and HbCOBL-N) were clustered as COBRA gene subfamily-I. By contrast, four genes (HbCOBL-O, HbCOBL-P, HbCOBL-E, and HbCOBL-L) were clustered as COBRA gene subfamily-II. The HbCOB subfamily-II was marked by the addition of 203 residues in C-terminal which is different with Arabidopsis. The gene HbCOBL-C was the putative ortholog to AtCOB carrying the unique COBRA domain cl04787 with 74 amino acid residues. Taken together, these results showed that Hevea and Arabidopsis COBRA genes might share similar functions while differ in gene structure.
... Some members in ethylene perception and signaling have been intensively investigated, especially ethylene response factor (ERF) transcription factors (Duan et al. 2010;Tang et al. 2016;Duan et al. 2013). Seven ERF genes were found to be highly expressed in latex and predicted to be involved in the regulation of latex cell metabolism (Piyatrakul et al. 2014), and three HbERF genes were dramatically accumulated by combining wounding, methyl jasmonate and ethylene treatments, and the induction was ethylene-dependent (Putranto et al. 2015a, b). In a recent paper, twenty-one of the AP2/ERF members showed a differentially expressional pattern after ethylene treatment (Tang et al. 2016). ...
Key message
Ethephon (an ethylene releaser) is commonly used to enhance latex productivity of rubber tree ( Hevea brasiliensis ), but the underlying mechanism has been elusive. The review presents the recent advances in understanding the molecular mechanism of increasing latex production in rubber tree by ethylene application.
Abstract
Rubber tree (Hevea brasiliensis) is currently the only commercial sources of natural rubber which is an important industrial material. Application of ethephon (an ethylene generator) has been a measure extensively adopted in worldwide rubber plantations to increase the productivity of rubber tree since the 1960s. In the recent years, adoption of genomic, transcriptomic, and proteomic approaches has brought great progress in understanding the mechanism of ethylene stimulation of latex yield. In this review, an update on the molecular mechanism of ethylene stimulation of latex production in H. brasiliensis is presented. Ethylene stimulation can be roughly ascribed to the acceleration of latex regeneration and the prolongation of the flow of latex. The relevant biochemical pathways and processes are comprehensively reviewed. The possibility that the limiting factors of the biosynthesis of rubber identified in bark glycolysis and photosynthetic carbon fixation can be utilized in molecular diagnostic and genetic engineering for rubber high-yielding variety improvement is discussed. Unsolved problems of the ethylene stimulation and a major challenge to understand the regulatory mechanism of the ethylene stimulation are also indicated.
... Characterization of the ethylene response factor (ERF) gene family in Hevea has led to the identification of several ERFs putatively involved in the regulation of redox genes (Piyatrakul et al. 2014). Their regulation by harvesting stress and their putative orthologs in Arabidopsis are presented in Figure 3. ...
... Otherwise, under reducing conditions and oxidizing conditions, the inactive transcription factor stays as a monomer or an oligomer, respectively (Shaikhali et al. 2008). This gene should belong to Hevea ERF group Ia (Piyatrakul et al. 2014), but to date there are no identified orthologues in the Hevea transcriptome. The new complete genome version is expected to provide additional genes that could include this gene (Tang et al. 2016). ...
... The biosynthesis of antioxidant compounds is also greatly controlled by ERF transcription factors. To date, no orthologous gene has been identified in rubber (Piyatrakul et al. 2014). In Arabidopsis, ERF98 activates the genes involved in the ascorbate biosynthesis pathway (Zhang et al. 2012). ...
Environmental stress can lead to oxidative stress resulting from an increase in reactive oxygen species (ROS) and involves redox adjustments. Natural rubber is synthesized in laticifers, which is a non-photosynthetic tissue particularly prone to oxidative stress. This paper reviews the current state of knowledge on the ROS production and ROS-scavenging systems in laticifers. These regulations have been the subject of intense research into a physiological syndrome, called Tapping Panel Dryness (TPD), affecting latex production in Hevea brasiliensis In order to prevent TPD occurrence, monitoring thiol content appeared to be a crucial factor of latex diagnosis. Thiols, ascorbate and γ-tocotrienol are the major antioxidants in latex. They are involved in membrane protection from ROS and likely have an effect on the quality of raw rubber. Some transcription factors might play a role in the redox regulatory network in Hevea, in particular ethylene response factors, which have been the most intensively studied given the role of ethylene on rubber production. Current challenges for rubber research and development with regard to redox systems will involve improving antioxidant capacity using natural genetic variability.
