MMR sequences identified in plant genomes
Plants are sessile organisms that are continuously exposed to different environmental factors, which may affect their development and production. In order to support this, plants change their metabolic pathways through different signal transductions in order to survive or set seeds to propagate the next generation [1, 2]. Due to this, it may be said that plants have a sophisticated perception of stress conditions. Moreover, these stress conditions might be biotic (caused by animals, insects, bacteria or virus), abiotic (caused by heat, temperature, drought, flood, salt, sunlight, soil contamination (chemicals mutagenic in soil or air), or endogenous metabolism (Figure 1). The response from plants to these conditions is usually associated with change in gene regulation, gene expression, protein translation, and post-translational modifications. These changes generated a change in plant metabolism, which is correlated to keep plant homeostasis, DNA repair, cell division, cell growth, and expansion [3, 4].
Regarding environmental conditions, plants are exposed continually to sunlight, which has a deleterious UV component. Then, in order to avoid this negative effect these organisms produce phenolic compounds such as flavones to reduce the amount that reaches the plant cells and they have DNA repair pathways to correct lesions and then keep the genome integrity [5-7].
In general, biotic or abiotic stresses are correlated with an increase in the Reactive Oxidative Species (ROS), and this has been associated as a type of oxidative stress . ROS may be produced due to oxygen presence during plant metabolism (photosynthesis), or a consequence of biotic and abiotic stress. The presence of ROS may produce other forms that are more reactive such as superoxide, H2O2, OH-, and singlet oxygen [8-9]. Normally, plants keep a balance between ROS production and degradation with an antioxidant system [9-10]. This system is formed by superoxide dismutase (SOD), catalase, and ascorbate peroxidase (APX) and others proteins. Furthermore, when plants are exposed to a stress condition (biotic or abiotic), the ROS production is accelerated and then a different physiological response [9-15]. It has been observed in some crops that the oxidative stress unbalances the ROS equilibrium in cells that may promote growth reduction, late development, decrease seed production [11-15].
When the ROS fine balance is not maintained, then these molecules may interact with DNA and this may produce DNA lesions and lipid peroxidation in membranes [9, 13-15]. Then, in order to avoid the DNA lesions and keep the genome integrity, plants have different DNA repair pathways to detect DNA lesions and correct them [15-16]. The effects of biotic and abiotic stresses on DNA repair have been observed (Figure 2).
“Omics” are a powerful tool to identify genes/proteins/metabolites that are involved in the plant response to a specific stress and/or to a DNA repair pathway . Besides, transgenic and mutant plants are also helping in the gene characterization function. The data have shown that plant response is more complicated than previously thought. Not only is the presence of transcript (tissue or time presence) important, but also the signals are important for gene regulation, post-translation modifications (ubiquitination or sumolation), protein degradation, and protein targeting. All these may change when plants are exposed to different environmental conditions [19-23]. Furthermore, the
Considering the importance of the plants for food production, it is important to identify which genes/proteins/pathways are involved in these different mechanisms. This knowledge is important for plant breeders to produce new cultivars [17, 28]. Moreover, considering all that was explained above, plants are an interesting model to study stresses and DNA repair (Figure 2) due their sessile condition, genome plasticity, and the fact that these organisms do not have a germinative cell lineage. The apical meristem cells (shoot or root) suffer division continually during plant development and then genome integrity is extremely important . Then, this chapter will focus on DNA repair pathways in plants.
This figure illustrates different abiotic factors such as drought, heavy metals, light, heat, ozone, lack of nutrients, cold, freezing, etc. Plants are able to perceive these different conditions or signals (on the right side) and then promote different molecular and physiological responses, which involve changes in gene expression, protein translation, post-translation modifications, degradation, epigenetic changes, and miRNAs. All these together produce a plant response that helps plants to tolerate this stress condition. Represented on the left side are the effects of an imbalance of ROS in DNA repair and the different DNA repair and genes that are involved in these different processes. The DNA repair presented in this figure includes mismatch repair (MMR), excision repair (NER and BER), and double strand breaks (HR and NHEJ).
Due to the sessile habits of plants, they are exposed continually to sunlight that is composed by UV-A (315 – 400 nm), UV-B (280-315 nm), and UV-C (200 -280 nm). However, due to the ozone layer, the UV-C does not penetrate. Furthermore, it is known that UV-B light affects photosynthesis, reduces productivity, and is also responsible for promoting lesions in DNA, such as (6-4) photoproducts and cyclobutane pyrimidine dimmers (CPDs). Moreover, plants produce compounds such as phenol compounds that act as filters in order to reduce the UV light in plant cells . Besides this, plant DNA also suffers DNA lesions. In rice cultivars was reported that CPDs may be the principal lesion that affects growth . In
The cryptochrome/photolyase superfamily (CPF) is a group of flavoproteins that includes photolyases and cryptochrome (CRY). Photolyases are DNA enzymes that are activated by light and when they recognize the CPD lesion, they are called CPD photolyases; and when they recognize the (6-4) pyrimidine-pyrimidone photoproducts, they are called (6-4) photolyases. CRY proteins do not have DNA repair activity, but they have a photoreceptor or transcription regulation functions . Moreover, by phylogenetic analysis using the genomic data available, the CPF superfamily was divided into the following groups: 1- Class II CPD (involved in CPD DNA repair); 2- Class I and II CPDs and CRY photoreceptors (blue light receptors involved in circadian clock regulation; plant development); 3- Cry DASHs (proteins that are able to do DNA repair); and 4- 6-4 photolyase (diverse group of proteins that includes DNA repair, photoreceptors, and transcriptional regulators) . Although CPF is a diverse group, these proteins have a conserved photolyase homology region (PHR), with two non-covalent bound chromophoros (FAD and 8-HDF/MTHF). The CPFs may also have an N or C-terminal extension that might be associated with different functions such as signalling, regulation, post-translational modifications, protein targeting, circadian clock regulation [30, 32].
It has been shown that some rice cultivars have different UVB sensitivity, which is related to CPD lesion, photolyase activity, and ability to correct these lesions [29, 36]. It was observed that overexpression of photolyases increases biomass production under UV-B light in
3. Mismatch repair — MMR
The mismatch repair pathway is important for the genome stability during replication and it has been associated with the correction of the incorrect base incorporation by DNA polymerase during DNA replication or during the process of recombination [1, 49, 50] as well as to correct the photoproducts [42-43]. The other function of this pathway is to reduce recombination events between diverged genomes [42, 44-45].
It has also been observed that MMR is conserved from bacteria, yeast, humans, and plants. This pathway is formed by the following proteins: MutS (recognizes the base-base mismatch and deletion or insertion that promotes mismatch on a DNA strand, ATPase activity); MutL (interacts with MutS, helps in the mismatch detection, recruits and activates MutH, ATPase activity); MutH (an endonuclease - identifies the hemi-methylated sequence and produces a nick on the DNA strand); DNA helicase II (MutU or UvrD); exonucleases (ExoI, ExoVII, ExoX, RecJ); SSB protein (single strand-binding protein); PCNA (important for lagging strand); DNA polymerase III (fill the gap), and DNA ligase (ligates the DNA ends) [41, 47]. Also observed in human cells hemi-methylated sites that may act as important signals for discriminating the strand where nicks is produced. Despite this conservation, some differences have been observed between bacteria, yeast, and humans, and plants, which may be related to the life style where plants are sessile organisms [41, 46].
One model for the MMR pathway is: MutS/MSH (this complex recognizes mismatches or insertions/deletions on the DNA strand and bind to the DNA strand); and MutL/MLH (this complex has been associated with ligation to the DNA strand and the DNA repair complex is assembled). The MutL/MLH protein complex interacts with MutS in helping the detection of the mismatch and the complex assembling. Then, both proteins activate the MutH protein. This protein now will recognize the hemi-methylation strand and produce a nick in the unmethylated DNA strand in a process that requires ATP-dependent proteins [41- 42]. After these steps, there is the association of PCNA, DNA helicases II, exonucleases, SSB, DNA polymerases, DNA synthesis and DNA ligation; then the mismatch lesion will be corrected. One difference between bacteria and eukaryotes is that MutS and MutL proteins work as homodimers and in the case of eukaryotes these proteins work as heterodimers (Table 1) [41-42].
This MMR pathway is able to identify a mismatch on the DNA strand, remove it, and replace it with the correct base [1, 40, 42]. Mutants in mice have shown that MMR proteins are associated with cancer as well as fertility as some mice mutants were sterile, and then it has been suggested that the MMR may also have a role in meiosis . As plants are sessile organisms and do not have specific germ cells, these organisms have meristematic cells that divide to form gametes. These meristematic cells go through division during the life cycle of the plant and then these cells may accumulate spontaneous mutations that need to be recognized and corrected in order to keep the genome integrity. Due to this aspect, MMR has an important role in the plant genome [1, 40, 42].
The genome projects have allowed researchers to identify gene sequences and it has been observed that in plants some MMR genes were duplicated when compared to a bacteria genome (Table 1). Phylogenetic work on MSH proteins (bacteria MutS homolog) has observed the division into two distinct groups . The idea is that the MutS from eubacteria present in mitochondria suffered duplication, and this new copy was transferred to nuclei where other duplication and specialization processes gave rise to MSH2, MSH3, MSH4, MSH5, and MSH6 in the nuclei. It has been observed that these sequences were related to recognizing and correcting DNA replication errors, and some proteins became involved in meiotic recombination. It has been proposed that these events occurred before the evolution of plants . Furthermore, it was observed that sequence from MSH7 is specific to plants (Table 1).
Considering the role of MMR in recombination, in
For the MSH genes, it has been proposed that MSH2 is an important gene for MMR pathway and for the recombination repression . This protein has a role in recognition of mismatch lesions (Table 1) and it forms dimmers to MSH3 or MSH6 proteins. The mutation only in the MSH2 sequence increases the homologous recombination by ninefold . It has been observed that mutants in the MSH2 gene had problems in setting seeds and siliques were abnormal; embryo lethality was also observed. These phenotypes suggested that these mutants probably accumulated many mutations, as it was not able to correct mismatch errors from DNA replication or normal metabolism .
In maize and in
The MSH7 protein (specific to plants) may interact to MSH2 as well as MSH3 and MSH6 . It has been shown that this protein plays an important role in maintaining the genome integrity in plants and meiotic recombination [49; 54]. In tomato plants was showed a role of MSH7 in anti-recombination activity . It was also shown that the heterodimer MSH2-MHS7 was able to recognize G/T or A/C mismatches, and this heterodimer may have a role in mismatches that arose from cytosine deamination or by UV or oxidative lesions .
The heterodimer MUTLα (MLH1-PMS1) has been considered an important heterodimer. The MLH1 has been associated with homologous recombination, as a decrease of 72% was observed . Mutant plants for this sequence had problems in setting seeds, and a problem in pollen formation has also been observed. Then, it was proposed that the MLH1 gene may be important for recombination as well as in limiting the recombination frequency between diverged sequences . For MLH2 it was observed that mutants also had problems in recombination, but the frequency reduction was only 22% . The MLH3 mutants also had a reduction in seed production, but also a verified decrease in frequency of crossovers. MLH3 has a role in meiosis and is expressed in reproductive tissues. The immunolocalization identified the presence of this protein as foci on the chromosome axes during prophase I in meiosis, suggesting a role in Holliday resolution. Furthermore, AtMLH1 protein is dependent on AtMLH3 protein . For the
The comparative genome analysis between
|MSHα – MSH2-MSH6||mismatch error and 1-2 bases of deletion/insertion loopout|
|MSHβ – MSH2-MSH3||2-12 bases of deletion/insertion loopout|
|MSHγ – MSH2-MSH7||preference for G/T or A/C base/base mispairs and meiotic recombination|
|MUTLα - MLH1-PMS1||endonuclease activity, protein/DNA complex|
|PCNA||Interacts with MSH2, MLH1, MSH6|
These data in plants showed the importance of MMR components and that many of these mechanisms are not clear yet, especially related to meiotic recombination and homeologous recombination.
4. Base Excision Repair (BER)
This pathway is responsible for identifying and correcting lesions associated with alkylation, oxidation, deamination, DNA replication, and base adducts that sometimes block DNA replication and transcription [59-60]. This pathway is a multistep, beginning with the lesion recognition by DNA glycosidase. These enzymes remove the base by an incision on DNA strands at the N-glycosidic bond that connects the base to the deoxyribose-phosphate residue. Then, this incision creates an abasic site or AP site [61, 62]. There are different DNA glycosylases (mono or bifunctional), each one specific to a different type of base lesion. The AP sites may also be produced by spontaneous depurination or by hydrolysis of N-glycosidic bond . After that, the AP site is processed by a bifunctional DNA glycosylase (3´AP lyase function) or by AP endonuclease. This excision creates a gap, which is filled with nucleotides by DNA polymerase and then ligated to the DNA strand by DNA ligase (Figure 3) .
The BER may be divided into two pathways: short-patch and long-patch (Figure 3). Choosing the short or long patch will be associated with which type of lesion and which DNA glycosylase will be used in the DNA repair. The short patch is responsible for correcting the lesion of only one nucleotide, and the long-patch will correct a lesion from 2 to 13 nucleotides . The other difference is that in the short-patch the DNA polymerase that acts in this process is Polβ (mammals) or PolI (bacteria) ; and the DNA sealing is done by XRCC1 and LigIII (mammals) or LigI (bacteria) [66-67]. It is known that for the long patch Polβ probably introduces the first nucleotide, but the other nucleotides are processed by Polδ or Polε . The short and long-patches were discovered by
Different work using the
The other interesting component of this pathway is the enzyme fosfodiesterase-DNA tirosil (TDP1), which is involved in the repair of lesions
Another difference observed in plants is related to AP endonuclease. This protein is necessary for survival, as it has been observed that homozygote knockout mice are lethal. . Furthermore, APE1 (also known as HAP1 or APEX) has two types of functions – AP endonuclease and a redox function to
The short-patch needs the DNA polymerase β and DNA ligase III, but as these sequences were not identified in
The first step of the BER pathway is the recognition of the lesion (represented by a star on the DNA strand). This lesion recognition is done by a bifunctional DNA glycosylase that makes an incision on the DNA strand and produces an end with 5´P and the other end 3´P or a 3´polinsaturated aldeid (PUA). In the case of the monofunctional DNA glycosylase, the nick is done by AP endonuclease creating 3´OH and 5´dRP. These ends were corrected by Polβ (dRPase function). The short-patch (left side) Polβ adds one nucleotide, and then XRCC1/LigIII or LigI does the ligation. In the long-patch Polβ and/or Polδ/ε adds the nucleotides (2 to 13); then the lesion is removed by the DNA Flap (FEN) and DNA is sealed by LigI. All the proteins and steps present in BER are represented by gray, and the proteins and steps present only in plants are represented by green color.
5. Nucleotide excision repair
Nucleotide excision repair (NER) is the other DNA repair pathway that removes damages caused by UV radiation and bulky covalent adducts that cause helix distortion [5, 93-95]. Furthermore, it has been observed that NER proteins are more conserved considering amino acid identity than the other pathways when compared with bacteria, yeast, humans, and plants .
NER is divided into two sub-pathways, each one having distinct damage recognition mechanisms but both using the same machinery to correct the lesion. Transcription-coupled repair (TC-NER) is responsible for the removal of lesions from the transcribed strand of actively expressed genes . This pathway is activated when RNA polymerase is stalled during transcription and it depends on the recruitment of the proteins CSA and CSB (Cockayne syndrome A and B) to the site of the lesion . This process was first discovered in mammals  and
The regions in the genome that are not actively expressed are repaired by Global Genome repair (GG-NER). In this case, the lesion is detected by the DDB2 (damage-specific DNA binding protein 2)-DDB1-CUL4 complex. The binding of this complex recruits another complex of proteins composed by XPC (
For both NER pathways it is important that the TFIIH complex (transcription elongation factor-IIH) unwind the DNA near the lesion site. XPB and XPD proteins are the subunits of this complex that have helicase activity . Orthologs of these two helicases were isolated in
In rice, differential modulation was reported for the genes
In the study  it was observed that OsREX1-S (a TFB5 homolog in yeast and human - a subunit of TFIIH), is involved in NER as it was observed that
Plants also have DNA polymerases that are an important component of the DNA repair machinery. The only family of these proteins known to have a role in DNA repair and recombination is the DNA polymerases X family . It was observed that AtPolλ had the C-terminal and N-terminal motives characteristic of the PolX family . Seedlings from two mutant lines for
6. Double-Strand Break (DSB) repair in plants
Double-strand breaks (DSBs) can be introduced in DNA mainly by metabolic products, ROS, radiation, replication, or transposon excision [119-120]. This structure is also intermediate in several recombination events in eukaryotic cells . When a DSB is detected in the cell, the cell cycle is stopped or arrested for its damage to be repaired  to avoid the serious consequences to the cell that an unrepaired DSB can cause, such as chromosome rearrangements, chromosome loss, or cell death . Prokaryotes and eukaryotes have evolved two main pathways to repair DSBs: non-homologous end joining (NHEJ) and homologous recombination (HR) [121-122].
6.1. Non-Homologous End Joining (NHEJ)
NHEJ promotes the ligation of two DNA ends without homology between them. If the DNA damaged is repaired by this pathway, the integrity of DNA molecule is re-established, but the sequence is altered because of the nucleotides additions or deletions at the junction . In plants, as in all the higher eukaryotes, DSBs in somatic cells are mainly repaired by NHEJ, but depending on the conditions of the cell, like the phase of the cell cycle and availability of homologous repair templates, DSBs can also be corrected by homologous recombination (HR) [120, 124]. Bacterial homologs of all DNA repair pathways were found in the genomes of
Another process of error-prone DSB repair was reported by direct ligation of extremities of DNA, without the participation of the KU proteins—microhomology-mediated end joining (MMEJ). This pathway uses a microhomologous sequence with the length of 5-25 base pair (bp) in the alignment of the DNA ends, before the ligation, which causes deletions in the flanking region of the DSB .
It was recently reported that PARPs (Poly-ADP-ribose polymerases) are involved in several processes and play a role in MMEJ in
It was verified in rice that the NHEJ pathway is involved in the
6.2. Homologous Recombination (HR)
HR is a repair pathway that uses a homologous donor molecule, being, in principle, a DSB repair pathway which is not mutagenic, since all the genetic information can be recovered in the case that the sequence of the template is identical to the broken site . In the HR process many proteins are recruited. PARP1 and PARP2 proteins are considered a sensor for DSBs and then these proteins are important for the recruitment of the MRN complex, which consists of MRE11–Rad50–NBS1 [139-140].
One of the proteins from the MRN complex,
For the homologous recombination process, it is important that a stretch of single strand DNA (ssDNA) be produced before the strand invasion. A 5´-3´degradation of DSB occurs, generating 3´ssDNA overhangs. This process is called end resection and it requires the action of nucleases and helicases. In yeast and mammals the kinases MEC1/ATR, TEL1/ATM, Rad53/CHK1, Cdc5/PL, and CDKs (cyclin-dependent kinases) are involved in this process . Five RAD51 paralog proteins are involved in the process of recombination repair in mammals: RAD51B , RAD51C , RAD51D , XRCC2 , and XRCC3 . RAD51C-XRCC3 form one complex and RAD51B-RAD51C-RAD51D-XRCC2 form another complex . In addition to these five genes,
During HR, in a few cases, there is a second strand capture after the strand exchange, forming a structure called Holliday junction (HJ) that consists of four DNA strands of two homologous chromosomes or sister chromatids . The removal of this structure is important to correct chromosome segregation. The enzymatic processing of recognition and cleavage or resolving these structures is done by resolvase proteins [157-158]. In
One important aspect for plant survival and reproduction is the accurate transmission of chromosomes during meiosis. The
7. DNA repair in organelles
Plants need to maintain the genome stability of the DNA in three compartments: nuclei, mitochondria, and chloroplast. The endosymbiotic theory postulates that these organelles originated from a prokaryotic organism that developed a symbiotic relationship with a eukaryotic host. In the course of time, chloroplast and mitochondrial genomes have been reduced and studies have shown that the nuclei genome integrated DNA from these organelles’ genomes.
Many studies have been done on nuclei, but little is known about plant organelle DNA repair (mitochondria or chloroplast) [15, 31]. Comparative analysis proposed that in the
7.1. Photoreactivation (DR)
This pathway may be an alternative mechanism to correct NER lesions. It has been shown that DR is functional in mitochondrial and chloroplast plant genomes. It was observed that CPDs and 6-4 photoproducts were corrected after
In plant organelles the BER pathway is also not completely understood. Some data have shown that this pathway occurs in mitochondria and chloroplast. It has been observed that the 8-oxoG lesion in mitochondria needs the OGG1 protein to correct it. Furthermore, it was verified that the mitochondria and chloroplast have a functional Uracil-DNA-glycosylase (UNG) . Furthermore, there is also the presence of thymine glycol DNA glycosylase proteins . In relation to AP endonuclease, it was verified in
With regard to short or long patch pathways, at least the short patch was detected in mitochondria . And for chloroplast, it was identified the presence of two homologs for endonuclease III and one AP endonuclease . For DNA polymerase γ, duplication was observed: POLγ1 (At3g20540) and POLγ2 (At1g50840). Both sequences had a dual targeting – chloroplast and mitochondria. On the other hand, it was observed for DNA ligase 1 an alternative splicing producing proteins that were targeting nuclei and mitochondria, but it is not clear about chloroplasts .
The role of the MSH1 sequence was analyzed in
7.5. NHEJ and HR
Furthermore, it was identified in the
Despite the existence of the homologous recombination DNA repair pathway in mitochondria and chloroplasts, it was verified in
The genomic comparative data from coding and non-coding sequences from the mitochondria genome of two
8. Plant-specific factors involved in DNA repair
Triggering the DNA repair machinery in response to lesions in DNA is essential in order to maintain the genome integrity . The cell cycle may be arrested to allow that the DNA damage is repaired before entering the mitosis process. The perception of DNA damage activates proteins that promote the suppression of the cyclin-dependent kinase (CDK) activity and consequently arrest the cell cycle process . B-type CDKs (CDKBs) are plant-specific, under cell-cycle control, and divided into CDKB1 and CDKB2 .
Endoreplication or endoreduplication is a common modification of the cell cycle, which consists of multiple rounds of replication from the nuclear genome without cytokinesis . A genotoxic stress may promote endoreduplication in plants and animals, but the function of this process in animals remains unclear, as endoreduplication can block mitosis and may be associated with tumor progression . In plants, the process of endoreplication is important, as it may be observed in
One of the largest families of plant-specific transcription factors is NAC, and AtSOG1 is one of the proteins that belong to this family . AtSOG1 protein has been associated with transcription, cell-cycle arrest and programmed cell death, and genome stability . Although there is no similarity in p53 and
ATAXIA TELANGIECTASIA MUTATED (ATM) and RAD3-RELATED (ATR) both are protein kinases that act as DNA damage sensors in mammals . In
The work  described MAINTANCE OF MERISTEMS (MAIN), one of the 14 members of the DUF1723 protein family in
Plant mitochondria present a striking homologous recombination activity . Therefore, this organelle has plant-specific ssDNA-binding proteins that function in this process like the Organelle single-strand binding protein (OSB)  and the WHIRLY protein (WHY) . OSB1, in
9. DNA damage in plant cells
Stem cells in plants are maintained in two regions: shoot apical meristem and root apical meristem, both of which may be referred to simply as meristem. The division of meristem allows plants to grow continually and produce new organs and tissues. These cells may divide for self-renew and also may produce new tissues and organs throughout their lifetime. For example, in shoot apical meristem these cells may produce leaves during the vegetative stage; however, when the plant reaches the reproductive stage, the meristem now produce flowers . Furthermore, like animal stem cells, plant stem cells are kept in microenvironments known as stem cell niches, where signals act to organize and keep the adjacent stem cells . In animals, it is known that stem cells have a low tolerance for DNA lesions. This process leads to apoptosis in order to avoid cancer and protect germline. In plants this process, as well as the tolerance for DNA damage accumulation at meristem cells, is not well-known . There are some differences between animals and plants with regard to programmed cell death (PDC), as some genes/proteins have not yet been identified [202-204]. It has been observed that PDC is dependent on ATM and ATR .  identified the
Considering that plants are sessile organisms, they are exposed to different environmental conditions (abiotic and biotic stress) as well as exogenous mutagens that may increase ROS, which may induce DNA lesion and increase the accumulation of DNA mutations in cells as described above.  worked with Arabidopsis mutants at the MMR pathway in order to test the genome maintenance and integrity. They observed in
10. Final considerations
DNA repair has been studied since 1970 in bacteria, but in plants the first gene was cloned only in late 80. Then, the worry about the ozone layer reduction and UV light that may affect plant production, DNA repair in plants came to have a place in this field. Genomics and comparative genomics were powerful tools for searching for homologous sequences in genes or proteins in plant genomes that are well characterized in bacteria, yeast, and humans. This data allowed identifying that many gene or protein sequences were also present in plant models such as
Then, all these data presented here show how important endogenous and exogenous signals are for the plant response and how these signals are connected to make a interconnected network that helps plant make the fine adjustment in their metabolism in order to tolerate the adverse conditions to which these organisms are exposed continually. Moreover, plants have become an interesting model for research because of their sessile style, photosynthesis, the ROS presence and a possible connection among ROS x stress x DNA repair x food importance. Much progress has been made, but a lack of knowledge still remains; consequently, much work needs to be done.