The bridge between genotype associations and innovations for Leptocybe invasa resistance in Eucalyptus: a meta-analysis

doi:10.21203/rs.3.rs-2090222/v1

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The bridge between genotype associations and innovations for Leptocybe invasa resistance in Eucalyptus: a meta-analysis

https://doi.org/10.21203/rs.3.rs-2090222/v1

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I. Background:

Plant phenotyping has been a bottleneck for selecting insect-resistant plants in breeding programs. Our objectives were to: use text-mining tools to investigate state of the art about Leptocybe invasa in Eucalyptus; identify associated molecular interactions involving genes as a candidate and their impact and associated metabolites pathways and determine how products are currently used to control this insect as patents.

II. Methods and Results:

The literature survey was explored by title, abstract, and keywords of scientific articles, a database of genes and protein sequences, and patents. Nucleotide and protein sequences were mined in public banks. In the literature, we searched for homology to known genes or predicted proteins with sequences described in Eucalyptus sp. To obtain a broad set of studies, we accessed literature data of the last 20 years conducted with combinations of search terms “Leptocybe invasa” OR “eucalyptus gall wasp” AND “control”. Patents were prospected and analyzed using Orbit Intelligence patent research software

III. Conclusions:

Succinct interpretation of results as well as significance of findings. Statement There are perspectives to access the genotype resistance; furthermore, it is critical managing the evaluable information as state of the art to overcome the damages of L. invasa beyond the genotype selection. The target genes found in this research can serve as a basis for further functional characterizations of Eucalyptus genes possibly related to response expression to L. invasa.

gene

bioeconomy

transcription

protein

The forests have a role in reducing natural disaster hazards, including floods, droughts, landslides, and other extreme events [1]. Otherwise, in the face of demands for technologies addressed to achieve the goals of sustainable development, the planted forests of Eucalyptus are the source of the broadest hardwood grown in the world because of its increasing importance for fiber and energy [2, 3]. Biomass of Eucalyptus is a versatile energy source, due to its fast growth, mainly used by the pulp and paper industry [4, 5]. The use of this species is based on recognizing the growth of bioenergetic demand and the existing pressure on natural resources by the lignocellulosic biofuel industry. Eucalyptus can become an important raw material for producing renewable fuels [6, 7]. Its versatility can be further attributed to the increased demand for alcohol gel sanitizer during the COVID-19 pandemic. As an alternative, there was an expansion of norms to produce alcohol gel sanitizer, allowing the use of other gelling agents, including eucalyptus byproducts. It has been proposed to use an alcohol gel formulation from mechanically defibrillated nano cellulose (MFC), as it is cheaper than existing products, has forestry origin, is affordable, and is available on a large scale [8]. The importance increases due to the accumulation of petroleum products that causes damage to ecosystems, which can be avoided with cellulose-based products [9], which could be minimized with cellulose-based products [10, 11]. However, in this crop, there is a particular concern with an insect attack denominated Leptocybe invasa pest Fisher & La Salle 2004 (Hymenoptera: Eulophidae), known as eucalyptus gall wasp [12]. The species exhibits the behavior of endophytic oviposition, inducing galls on leaves, petioles, and young branches of eucalyptus [13]. The damage caused by this insect has harmed forestry on a large scale, decreasing productivity, altering photosynthesis, and impacting tree development [14, 15, 16].

There are several hybrids of diverse eucalyptus species susceptible to gall formation (Eucalyptus camaldulensis, E. saligna, E. botryoides, E. bridgesiana, E. cinerea, E. dunni, E. globulus, E. grandis, E. urophyla, E. gunni, E. longistrata, E. major, E. nicholli, E. propinqua, E. pulverulenta, E. robusta, E. rudis, E. tereticornis and E. viminalis, E. smithii, E. moluccana, E. coolabah and E. pellita [17, 18, 19, 20]. However, eucalyptus species and their hybrids resist gall formation [21]. Thus, obtaining information that establishes appropriate control strategies to reduce productivity losses in the forestry sector is essential. Eucalyptus species' ecological and economic importance remains understood considerably by the biological interaction between insects and plants [22]. This knowledge has important implications for predicting regions that may be vulnerable to future pest invasions and understanding the accumulation of pests outside the native ranges of their hosts [23]. An alternative is searching for genetically resistant organisms, mainly through the prospection of genes to subside genetic breeding. Qualitative resistance genes, known as R genes, are part of the detection mechanism of foreign organisms, such as pathogens, by interacting with the avirulent gene (Avr) after the attack [24, 25]. Recognition proteins encoded by R genes are predominantly intracellular receptors with high target specificity. Nucleotides' recognition and subsequent binding lead to responses interrupting pathogenicity [26].

Most of the resistance genes that have been cloned and characterized resemble constituents involved in signal transduction. These can be categorized into five classes based on the protein structure of the domains Kinase, Leucine-Rich Repeat - LRR, Nucleotide Binding Site - NBS, Toll/interleukin-1 receptor/resistance protein – TIR, and Transmembrane Domain - TM [27]. All five classes of R genes with their respective conserved domains are expressed in eucalyptus. There are 19 genes with potential resistance to diseases: Pto, Bs2, Gpa2, I2, Rxl, Rx2, Sw5, Xa1, RpI, MiI, L, M, N, P, RppI, Rpp5, Rps4, Cf4, Cf5, and Xa2I [28]. These molecular patterns are identified by the pattern recognition receptors (PRRs) in the plant cell, and trigger defense responses as the plant perceives them as indicative of a pest attack [29]. There are PRRs for sensitive and rapid detection of potential danger. Plant PRRs are either surface-localized receptor kinases (RKs) or receptor-like proteins (RLPs) containing various ligand-binding ectodomains that perceive pathogen-associated molecular patterns (PAMPs) or damage-associated molecular patterns (DAMPs) [30, 31].

Studies have identified gaps in developing technologies to control eucalyptus gall wasp [32, 33, 34, 35]. Seven significant loci have been detected associated with resistance to L. invasa in Eucalyptus grandis, of which five Embra333, EUCeSSR0930, Embra321, EUCeSSR479, and EUCeSSR683 are homologous to known genes or predicted proteins [36].

The main goal of our study is to prospect data on potential gene expression, and aiming allows approaches in the process of metabolic reconstruction and the functional prediction of their action. Therefore, this work aims to map scientific studies on gene expression and insect control; and technological products to control gall disease (L. invasa) and to identify perspectives for its management in Eucalyptus sp.

Review Procedure

To obtain a broad set of studies, we accessed literature data of the last 20 years using Scopus (http://www.scopus.com) and Web of Science (http://www.webofknowledge.com) conducted with combinations of search terms “Leptocybe invasa” OR “eucalyptus gall wasp” AND “control”. Scientific Articles were screened using keywords in the title and abstract. The data were evaluated to ensure each study met the criteria of containing quantitative data about L. invasa. The search was restricted to publications (articles) and records identified from databases Scopus (n = 36) and Web of Science (n = 210) and resulted in 246 registers. We removed the duplicated articles (n = 57) before the screening. We retrieved the abstracts of 189 articles. In the end, 88 records were eligible for more accurate analysis [37]. The meta-analysis was conducted using R 4.0.0 [38] and RStudio 1.1.463 software [39]. They were combined into a single database and examined with the Bibliometrix R-package [40].

Gene Prospecting (Dup: Abstract ?)

The nucleic acid sequences prospected in public molecular databanks as the Genetic Sequence Database-GenBank (http://www.ncbi.nlm.nih.gov/genbank) were evaluated, and fasta format was accessed from the homology to reach genes or predicted proteins linked to gall wasp resistance a Blastx against non-redundant data Eucalyptus.

Alignments were performed using Blastx against a non-redundant protein database to find similarities using Universal Protein (Uniprot) (https://www.uniprot.org/).

Alignments obtained with identity above 50% and e-value different from 0 were submitted to the String software (https://string-db.org/cgi) co-expression network for proteins with high similarity to those involved in the resistance to L. invasa. The QuickGo (https://www.ebi.ac.uk/QuickGO/annotations) was used to verify the correctness and justness of similar proteins and obtain functional annotations. An interaction network of the input genes to obtain co-expression and the alignments were performed using Blastx format FASTA. The alignments were performed using blastx against non-redundant data of Arabidopsis thaliana. The GeneMANIA platform was accessed to obtain genes related to a set of input genes, using a large group of functional association data, including proteins and gene interactions, pathways, co-expression, co-localization, and protein domain similarity [41].

Gramene (http://www.gramene.org) was used to identify metabolic pathways, chemical compounds, and proteins in response to stimuli caused by biotic stress in the Eucalyptus grandis. Gramene is software for comparative functional analysis of principal crops and model plant species. The information used was found in the Plant Reactome database, which hosts pathway data of 67 cultivated model-plant. Oryza sativa L. was used as a model species for inference and constructing parameters for Eucalyptus grandis. The original model is used as a reference for curating varietal pathways in other species' genetic ontology [42]. In the PubChem database (https://pubchem.ncbi.nlm.nih.gov/) were prospecting structures and molecular formulas of chemical compounds [43] that could be important in this study.

Patent Prospecting

Patent data was prospected and analyzed using Orbit Intelligence patent research software [44]. The covering publications were from 87 offices and databases: EPO - European Patent Office, WIPO – World Intellectual Property Organization, OAPI – Organization Africaine de la Propriété Intellectuelle, ARIPO – African Regional Intellectual Property Organization, EAPO – Eurasian Patent Organization e CGC – Chandigarh Group of Colleges.

Data from depositors, inventors, citations, international patent classifications and geographical and temporal distribution were processed. In the advanced search option, the terms “Leptocybe invasa” OR “eucalyptus gall wasp” were considered for documents that presented one of these words in the title, summary, and description. There was no temporal delimitation at this stage of the research.

The landscape map construction was extracted from the patents' full text and classified by technologies. They reflect the semantic content of the patent. The map was elaborated based on IP (Intellectual Property) Business Intelligence in four stages: construction of a vector model, clustering, size reduction, and design. Clusters were built by an algorithm that calculates the number of families for a concept and the relationship's similarity and proximity; then, families and positions were added to the map. Clusters represented the technical categories.

Systematic Review of literature

Two hundred forty-six publications have prospected in Scopus (36) and Web of Science (210). The duplicates were removed, totalizing 189 articles. The scientific journal denominated “Scientific Reports” there is a significant number of documents, followed by “Biological Control,” “Biological Invasions,” “Zootaxa,” and “African Entomology".” Biological Control” has the highest impact factor (H-index = 5). The journals “Zootaxa” (3), “Scientific Reports” (2), “Biological Invasions” (2), and “African Entomology” (2) also stand out, with a high impact factor.

China ranks first among the countries of origin of most of the corresponding authors with approximately nine authors, followed by Italy (7) and South Africa (6). These results could be supported because China is capturing intellectual rents from its increasingly transnational and technologically diverse innovation networks by leveraging its national innovation system [45]. However, the countries most cited in the manuscripts were South Africa with 145 citations, Australia with 110, and Uganda with 70. Numerous eucalypts (species in the genera Eucalyptus, Angophora, and Corymbia) have been introduced to South Africa and Uganda over the past two centuries. Several species have become naturalized or invasive and are the focus of control programs in South Africa. Many eucalypts species and genotypes are not easy to identify in the field, and the distribution patterns in the country are poorly documented. Besides providing new species records, the survey highlighted the paucity of information on the identity and introduction status of eucalypts in South Africa. A systematic study to provide an inventory of eucalypts and their introduction status for the entire country is needed to serve as the foundation for strategies to manage species to capitalize on their benefits and minimize their impacts [46]. Considering Australia, the importance is directed because this country is the center of the diversity of Eucalyptus.

The authors of the most cited studies were: Protasov (68), La Salle (45), and Mendel (32). It is significant to mention that Protasov, La Salle, and Mendel have publications. The publications related to the topic started in 2007. In 2008, a peak in publications led by the mentioned authors was represented in the bubble chart. The size of the bubbles is proportional to the number of publications, and transparency is inversely proportional to the amount of work. That same year the eucalyptus gall wasp was cited for the first time in Brazil. From 2014 onwards, there was an increase in the number of publications that remained until 2017 (Fig. 2).

The University of Pretoria in South Africa (22 documents), Guangxi University in China (7), and Tropical Forest Research Institute in India (5) are references in this kind of manuscript. The most relevant eucalyptus keywords were Hymenoptera (25) and the wasp (21).

Two co-occurrence networks were formed by analyzing multiple correspondences of the keywords to articles. Using this methodology is possible to plan state-of-the-art and to know the main lines covered by research (Fig. 3).

In Fig. 3, the first group (red) is represented by the host (Eucalyptus, species) and the insect (gall, wasp, parasitoid, Leptocybe invasa, Hymenoptera, Eulophidae). The second group (blue) addressed the management (biological, control).

Gene prospecting

Benefits from high-throughput sequencing may be most apparent for species with high societal or economic value but few genomic resources. Rapid means of gene sequence discovery provide a set of baseline tools for genome-level research. In Eucalyptus, the platforms are enriched by studies on E. grandis, E. camaldulensis, E. melliodora, and E. pauciflora, which sequences are available at the National Center for Biotechnology Information (NCBI). E. grandis genome was used for similarity and converted into proteins for data analysis using Blastx (Table 1). Protein-protein interactions are significant due to their versatility, specificity, and adaptability.

Table 1 Alignments sequences of Eucalyptus grandis, protein identity, score, e-value, and NCBI entry.

Gene	Protein	Identity (%)	Score	E-value	NCBI Entry
Embra333	Transcriptional regulator TAC1-like	97.1	178	2.2e-14	A0A1S2YMX8
	Transcriptional regulator TAC1-like	81.8	184	3.3e-15	A0A0B2SJS6
	C2H2 zinc finger domain binding	91.7	176	3.4e-14	A0A4P1REE4
	C2H2 zinc finger domain binding	84.2	175	2.9e-14	A0A072U0P2
EUCeSSR0930	C2H2 zinc finger domain binding	59.4	193	4.1e-15	A0A5N6MXE1
		58.1	194	1.3e-15	A0A118JWL3
		56.8	204	2.6e-16	A0A6A6K9B0
	Transcriptional regulator TAC1-like	56.5	198	4e-16	A0A6P6UAV3
Embra321	Reductase-like	95	99	1.6e-3	A0A6I9YQQ8
	Beta-ketoacyl-[acyl-carrier-protein] synthase I	91.3	104	3.2e-3	A0A251P8V8
	Serine/threonine phosphatase activity	80.8	105	2.1e-3	A0A3S1B8N6
	SART-1 family protein DOT2	80.8	103	3e-3	A0A6A4VE12
EUCeSSR479	1,3-(1,3)-beta-D-glucan 3-glucanohydrolase activity	73.2	2,698	0.0	A0A2I0L659
EUCeSSR683	Chloride channel protein	40.1	184	1.8e-12	A0A2A9MFC3
	Receptor-like kinase	40	189	3.3e-13	A0A7J6X339
	WH2 domain-containing protein	37.4	195	4.9e-14	A0A165I7B9
	WH1- domain-containing protein	36.4	202	5.9e-15	A0A165CII6

The Search Tool for the Retrieval of Interacting Genes (STRING) aims to integrate all known and predicted associations of proteins, both physical and functional [47].

The transcriptional regulator TAC1-like has conserved domains, and the Cys2His2 (C2H2)-type zinc finger protein may be involved in transcriptional regulation. By String, it was possible to obtain the protein-protein interaction of TAC1-type transcriptional regulator protein (Fig. 4).

In Fig. 4, it is possible to an overview of predicting functional co-expressed proteins and scores. LOC101515670, is a telomerase and, as a ribonucleoprotein, is essential for chromosomal ends replication in eukaryotes. Telomerase reverse transcriptase (TERT) and the noncoding telomerase RNA (TR) subunit constitute the core of telomerase. It has shown a score of 0.788 in the interaction network with LOC101492250, a Transcriptional regulator TAC1-like, followed by LOC101504854, the C2H2 binding zinc finger domain (0.707). The LOC101501419 is a DNA repair protein RAD50 (0.644); LOC101500768 is a pentatricopeptide repeat protein, At4g22760-like (0. 64); and LOC101498050 is a Trihelix transcription factor type GTL1(0. 613). LOC101494384– is a Elongator complex protein 3-like; tRNA acetyltransferase catalytic subunit of RNA polymerase II elongation complex, which is a component of RNA polymerase II (Pol II) holoenzyme and is involved in transcriptional elongation (0.613); and LOC101505905 - is a Phospholipase type A1-IIdelta-like (0.598) [48].

C2HC zinc fingers (AT4G17810) is a superfamily protein whose function is sequence-specific DNA binding transcription factor, zinc ion binding, and nucleic acid binding. It is involved in the regulation of transcription, which is an intracellular medium expressed in plant structures and expressed during growth. The predicted linkage between Protein Families (COGs) of Transcriptional regulator TAC1-like is based on observed co-expression of homologs in other species, which can be seen in Fig. 5.

The COG expression using the GUS reporter gene was observed in seedlings at young and mature leaves, restricted to the abaxial tissues. Gene expression was also observed on both sides of the leaf margin in young leaf tissues, with a co-expression association score of 0.409.

The overexpression of the ZFP11 protein induces death and a misshapen INO phenotype - essential for asymmetric growth of the outer integument of the ovule. Family Members of the YABBY protein of putative transcription factors contain Cys (2)-Cys (2) zinc-finger domains and regions of similarity to high mobility group (HMG) transcription factors. C2HC superfamily zinc-finger protein, a probable transcriptional regulator, is a cadastral protein that acts indirectly to prevent the B-class homeotic proteins and may fulfill the role of repressing genes implicated in cell division [48].

Proteins can form a variety of functional connections with each other, including stable complexes, metabolic pathways, and a bewildering array of direct and indirect regulatory interactions. These connections are networks, and the size and complex organization present a unique opportunity to view a given genome as more than just a static collection of distinct genetic functions. An interaction network of 20 related genes, with 21 total genes, presented 96 interactions, of which 52,06% are physical interactions, 21,72% predicted, 18,12% co-expression, 4,9% are protein domains shared, and 3% are genetic interactions (Fig. 6).

The co-expressed genes with AT4G17810 occur in the plastid thylakoid membrane, photosynthetic membrane, and chloroplast thylakoid. Description of the 20 networked genes presented in Tab. 2.

Table 2 Related genes with AT4G17810 - C2HC zinc fingers. Gene, ID gene and description [49, 50].

Gene	ID gene NCBI	Description
AT3G45880	823731	2-oxoglutarate (2OG) and Fe(II)-dependent oxygenase superfamily protein
AT2G21530	816692	SMAD/FHA domain-containing protein
ZHD6	9320196	Zinc-finger homeodomain protein 6
CRRSP11	110096294	Cysteine-rich repeat secretory protein 11
ATL66	109240015	RING-H2 finger protein ATL66
JAG	843177	Zinc finger protein JAGGED
AT4G23860	828485	PHD finger protein-like protein
ZFP8	818794	Zinc finger protein 8
STR4A	109207761	Rhodanese-like domain-containing protein 4A
MTERF2	9316461	Transcription termination factor MTERF2
AT2G38180	818396	SGNH hydrolase-type esterase superfamily protein
AT2G26340	817174	hypothetical protein, located in: chloroplast thylakoid membrane, expressed in 22 plant structures
AT3G56010	824767	Transmembrane protein
AT5G61190	836240	Putative endonuclease or glycosyl hydrolase with C2H2-type zinc finger domain
AT5G48830	834941	Phosphoglycolate phosphatase, located in chloroplast
AT4G12500	826862	Bifunctional inhibitor/lipid-transfer protein/seed storage 2S albumin superfamily protein
SECE1	827144	secE/sec61-gamma protein transport protein
IDD5	814738	Protein indeterminate-domain 5, chloroplastic
PTAC14	827759	Protein plastid transcriptionally active 14
HEMB1	843310	Delta-aminolevulinic acid dehydratase 1, chloroplastic

The information obtained in Tab. 2 allows us to understand how the L. invasa damages are so expressive in physiological pathways in Eucalyptus. The main involved in this damage is the chroloplasts, a vital organelle in plants.

From the inference based on the homology mappings of the Ensembl using Gramene, it was possible to have access to chemical compounds and their pathways linked to responses to stimuli caused by biotic stress in E. grandis (Table 3).

GTP is responsible for inducing changes in the conformation of macromolecules. When a GTPase: GTP receptor binds to a GTPase: GDP receptor, a conformational change is mediated that causes the guanine nucleotide exchange factor to induce the exchange of GDP for GTP in the α subunit (Fig. 7). They are active signaling molecules that initiate intracellular signaling cascades effects of hydrolyses. GTP as a control element allows cyclic variation in macromolecular form [51].

In the Plant Reactome database, 20 specific genes involved in response to stimuli caused by biotic stress in E. grandis were prospected: genes Eucgr.J01662, Eucgr.B02378, Eucgr.J02058, Eucgr.B03736, Eucgr.B02731, Eucgr.G03004, Eucgr.E00137, Eucgr.F03781, Eucgr.A01105, Eucgr.A01104, Eucgr.E03996, Eucgr.A01102, Eucgr.A01103, Eucgr.L03513, Eucgr.I01508, Eucgr.B03930, Eucgr.A01.268, Eucgr.A01. J00006, Eucgr.B02363. The results confirm the numerical and group complexity for thioredoxins (Trxs) genes already observed in the first Eucalyptus transcriptome. Genes have been identified for all described Trxs groups. Eucalyptus possesses at least 22 specific thioredoxin genes identified by comparative phylogenetic reconstruction. The numerical distribution of genes by groups is similar to that reported for Populus trichocarpa, showing the maintenance of 4 Trx m genes as in A. thaliana, instead of 8 in P. trichocarpa. The most abundant group in genes is represented by Trx h, with nine genes, and the expression profile of these genes revealed unique expression patterns not yet reported in eucalyptus. The Eucgr.F01604 gene, encoding a Trx h1, could play a somewhat significant role in conductive tissues, as well as relevant expression in young leaf tissues. This specific tissue expression was verified in semi-quantitative RT-PCR experiments. The expression of the Eucgr.I02383, Eucgr.I01913, Eucgr.F01854, and Eucgr.F01604 genes by RT-PCR confirms what is observed in silico. This genetic characterization, via differential expression of transcripts, indicates that future studies to obtain commercial transgenic plants with biotechnological potential using those genes are of interest. However, the need remains to conduct more experiments on the functional characterization of eucalyptus thioredoxin h in plantae [52]. The in-depth knowledge of these genes can serve as a basis for future work on responses to biotic stresses in Eucalyptus.

Patent Prospecting

Technological innovations may involve obtaining new drugs to control pests, such as L. invasa; and new engineered genes that could be patented.

In this context, there is an ongoing need for the discovery and development of new insecticides due to the loss of existing products through the development of resistance, the desire for products with more favorable environmental and toxicological profiles, shifting pest spectrums, and changing agricultural practices. Using the patent prospection methods could open frames to access state of the art and to overview new studies perspectives. Them the search carried out on the Orbit Intelligence platform, 420 patent documents related to gall wasp control were obtained, and 86 expired. The patented innovations for control of the gall wasp began in 2010 with four patents, two years after the first peak of scientific publications registers. The deposits increased in the following years, reaching 51 in 2014 and decreasing to 36 in 2015. In 2016 there was another increase, achieving the highest growth (60), followed by (51) 2017 and (54) 2018. China stood out in patent registration from 2013 to 2018 (heat chart). Brazil had an expressive number of publications from 2015 to 2018. The red indicates the highest frequency of country patents per year (Fig. 8).

Those data do not indicate new drugs but indicate that molecules to control gall wasp could be discovered in a country, but to be used worldwide, obligatorily need to be registered as patents in all countries that will be used. In this scenario, a landscape map was obtained to present the technologies associated with the patents. We identified seven groups: (1) Hetherocycle compound condensation, (2) Resistant pest, (3) Agricultural pest control, (4) Phytopathogenic pest, (5) Agricultural chemical formulation, (6) Olefin Polymer, and (7) gene expression. In the map, clusters are identified (groups) of families in different colors (Fig. 9).

In Fig. 9, each cluster represents an area on the map with several points of the same color, and the points correspond to a family. The same color for each cluster represents the names of the map's three most statistically relevant concepts. The distance between two points is proportional to two semantic concepts. The map interpretation is analogous to a topographic map. Private companies focused on the agrochemical sector are leading granting institutions for patents related to gall wasp control. The companies ROTAM (85), BASF (76), and Nippon Soda (40) are the prominent companies in the market (60%) (Fig. 10).

Approximately 1,740 records are addressed as patents. 31% of the company's product are insecticides [53]. BASF is a global German chemical company and a world leader in the agrochemical field, with a sales volume of 60 billion euros and more than 390 production units in more than 80 countries in 2019 [54]. According to the document entitled "The Global Economy in 2030: Trends and Strategies for Europe", in 2030, about two-thirds of the growth in global chemical production will come from China. The country is responsible for approximately 50% of the worldwide market [55]. Nippon Soda is a Japanese company and has offices in different countries. Brazil and China are its main agrochemical markets [56].

Technological domains are defined based on patent classifications by the International Patent Classification (IPC) [57]. The main products with a focus on eucalyptus gall wasp control are categorized asAO1N - Pesticides and biocides (250); CO7D - products obtained from organic chemistry (124), and A61P - medical preparations (63).

Focusing on genomic loci related to resistance to gall-inducing insects, they were identified for the first time on Eucalyptus species. Favorable alleles were potential molecular markers in marker-assisted selection for eucalyptus gall wasp resistance [36]. In addition, they can be analyzed using bioinformatics tools and help track genomic loci of interest, select markers for elite genotypes, and investigate the events that lead to resistance. The availability of E. grandis genomic sequence data makes it a valuable model for studying defense responses to current and emerging pathogens in various species of the Myrtaceae family [58].

Information on the biology and genetics of L. invasa may also contribute to the emergence of technological innovations, mainly in pesticide formulations, as shown in the present study. These formulations generally have side effects at the environmental level, and sustainable technologies are required. Most patents are related to the development of pesticide formulations [59, 60, 61]. An insecticide composition contains spiro treatment and ivermectin [62].

An invention discloses a volatile component exuded by (extracted from or produced by). This component attracts L. invasa Fisher and captures it in a viscose plate where the insect is induced to gather. The variation in the population of L. invasa can be monitored by the number of insects. It is inexpensive, simple, convenient, and friendly to the environment [63].

The primary innovation in RNA-mediated gene silencing in insect species. It is based, in part, on the sequencing of genes from Eucalyptus sp. of L. invasa (Li) and Ophelimus maskelli (Om) [64].

Based on transcriptome profiles of resistant and susceptible genotypes from an independent experiment, was identified several putative candidate genes in associated genomic loci, including Nucleotide-binding ARC- domain (NBARC) and toll-interleukin-1-receptor-Nucleotide binding signal Leucine-rich repeat (TIR-NBS-LRR) genes [65]. Structures, jointly with functional data, including identifying interacting proteins, have started to provide insight into the molecular basis of animal and plant immune signaling complexes’ assembly and host immune suppression by bacterial pathogens. This review focuses on the current knowledge of the structures of the TIR domains and how the structure relates to function [66].

All data about the R genes complement the previous information. The nucleotide-binding domain and leucine-rich repeat (LRR) gene family expand the plant lineage with extensive sequence and structure polymorphisms [67]. Protein sequences from seventy R genes from various cultivars were analyzed in which twenty-six proteins displayed zinc finger domains and nucleotide-binding sites leucine-rich repeat domains (NBS-LRR). Proteins fused with these zinc finger domains make them zinc finger proteins. These domains are required to function for individual proteins under stress conditions [68].

C2H2 zinc finger proteins are one of the plants' most prominent transcript factor families and have participated in diverse signal transduction pathways and developmental processes, including pathogen defense and stress responses [69]. Zinc finger proteins are categorized into nine subfamilies based on their conserved Cys and His motifs, including the Cys2/His2-type (C2H2), C3H, C3HC4, C2HC5, C4HC3, C2HC, C4, C6, and C8 subfamilies. Many C2H2-type zinc finger proteins function as transcriptional activators during plant growth and abiotic stress [70].

The C2H2-zinc finger protein (C2H2-ZFP) is essential for regulating plant development and is widely responsive to diverse stresses, including drought, cold, and salt stress, further affecting the late flavonoid accumulation in higher plants [71].

Zinc finger protein (ZFP) TFs have a crucial role in phytohormone response, plant growth and development, stress tolerance, transcriptional regulation, RNA binding, and protein-protein interactions. Recent research has revealed the regulatory and biological functions of ZFPs in incrementing plant resistance to pathogens [72].

There is an abscisic acid-responsive protein interaction network for sucrose non-fermenting related kinase in abiotic stress response [73]. An extracellular network of Arabidopsis leucine-rich repeat receptor kinases with physical interactions [74]. A comprehensive analysis of interaction and localization of Arabidopsis SKP1-like (ASK) and F-box (FBX) proteins [75].

Based on the knowledge generated about the families of identified transcription factors, it was possible to realize that some of these factors may present a relationship with already known responses to disease and pathogen attack. However, the predicted linkage between Protein Families (COGs) of Transcriptional regulator TAC1-like, such as C2H2 zinc finger proteins, still requires further studies on the processes in which they are involved.

GTP-binding proteins are fundamental molecular switches in eukaryotic signal transduction that cycle from a GTP “on” state to a GDP “off” state. Two main signaling G proteins are known: heterotrimeric G proteins and the RAS superfamily of small monomeric GTPases. The RAS superfamily is composed of five families (RAS, RHO, RAB/YPT, ARF, and RAN); however, only GTPases RAS and RHO are considered natural signaling proteins, while RAB/YPT, ARF, and RAN are directly involved in the regulation of vesicular or nuclear traffic [76].

G proteins are GTP-binding proteins with GTPase activity that act as molecular switches to regulate various cellular processes, alternating between an active (GTP-bound) and an inactive (GDP-bound) conformation. Small GTPases are widely conserved in eukaryotes and regulate many essential cellular processes [77]. Several RHO families of small GTPases are the primary regulator of immunity in plants and animals [78]. Thus, secondary metabolites formed from metabolic pathways linked to GTP can act in expressing responses to biotic stimuli.

The use of article information stood out as the focus of the study about the control of eucalyptus gall wasp. The potential use of articles, patents, and gene information is verified, and it is expected to direct efforts towards the emergence of research to enable the application of technological innovations.

The information obtained in this work expands the knowledge about the expression of genes targeted to identify eucalyptus resistance. The analysis of these genes may be of great importance for understanding the events that lead to plant resistance, constituting valuable tools for the development of studies involving the relationship of these genes with resistance to L. invasa and the appearance of symptoms associated with gall. In this study, the articles by literature review, associated with information about the state of the art of innovations (patents) and gene expression, could be utilized to obtain a comprehensive analysis of the resistance in plants and how the genes can be helpful in the selection of Eucalyptus genotypes resistance of L. invasa. It is an essential insight into the overall functional response against insect pests and diseases. Moreover, the evolutionary relationships, diversity, and expression profiles across different genotypes that could be tested were invaluable references for designing a practical framework for the new identification of Eucalyptus resistance breeding programs.

Eucalyptus is the most widely planted type of hardwood and represents a vital biomass source to produce its major components (hemicelluloses, cellulose, and lignin). The study uses articles, patents, and gene expression to establish diverse processing technologies. In terms of the weak and strong points, challenges and opportunities can reduce the insect economic damage by defining new approaches. An alternative is the search for genetically resistant organisms, mainly through the prospection of resistance genes, for use in genetic breeding with molecular markers-assisted selection. The target genes found in this research can serve as a basis for further functional characterizations of Eucalyptus genes possibly related to response expression to Leptocybe invasa.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Conflict of Interest

The authors declare the absence of any commercial or financial relationships that could be presented as a potential conflict of interest.

Author Contributions

CCC conducted the research and wrote the text, RSM guided the study, revised the text, and contributed to the writing of the manuscript, VVN and JLS contributed to obtaining the research data in the paper, translation, and revision of the text. All authors contributed to the article and approved the submitted version.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

We thank the Brazilian National Council for Scientific and Technological Development (CNPq), and Coordination for the Improvement of Higher Education Personnel (CAPES – Grant 001).

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

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The bridge between genotype associations and innovations for Leptocybe invasa resistance in Eucalyptus: a meta-analysis

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