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Byline: S. M. Jazayeri, L. C. Garcia Cruzatty and R. Villamar-Torres

Keywords: Arabidopsis, genes, genomic comparison, heavy metal, tolerance.


Arabidopsis is the reference model in plants The genome of A. thaliana published in 2000 (Arabidopsis Genome Initiative, 2000) has revolutionized the genomic era and provided a very useful source and reference for publishing genomes of other organisms from prokaryotes to eukaryotes. Homology among genomes and genes have answered many biological questions based on orthologues and revealed several life secrets but depending on the under study organism, its speciation divergence and convergence, gene annotation and function (Jones et al., 2008). There are 11 Arabidopsis species ( psis/) those possess different chromosome numbers and can be listed into 4 groups (Table 1). The chromosome number show how they have diverged during speciation process (Levin and Wilsont, 1976).

Despite of its importance in genus level for genetic and genomic studies in plant kingdom, the genome of only three Arabidopsis species have been published; A. thaliana (Arabidopsis Genome Initiative, 2000), A. lyrata (Hu et al., 2011) and A. halleri (Briskine et al., 2017). However, nowadays it is unavoidable to publish genome of other species to understand biological concepts, evolutionary mechanisms, and speciation events. Genomic data in plants provide necessary information for plant selection and are of help for understanding which biological mechanisms exist and revealing gene function and annotation (Jazayeri and Villamar Torres, 2017). The data generated by Arabidopsis model studies reveal that similar processes exist in other plants because of gene homology and orthology (Bauer et al., 2004). However, such similarities and differences among living organisms make biology interesting and informative (Jones et al., 2008).

As shown by chromosome number and 4 groups those were classified into two somewhere else (Koch and Matschinger, 2007), A. thaliana belonging to the Group1is the only species with 2n=10 separated from the rest of the genus (Table 1). The Group 2 comprises the species possessing 2n=16 including A. croatica, A. halleri, A. lyrata, A. cebennensis, A. pedemontana, as well A. neglecta, A. umezawana that are closely related species pairs (Bomblies and Weigel, 2010). A. arenosa, with 2n=26 and A. umezawana with 2n=32 belong to the Group3 and Group4 respectively suggesting that they are totally separated from the other species by genome duplication/deletion events (del Pozo and Ramirez-Parra, 2015). However, as the genome of all species is not published yet, it remains unclear how they have separated from their ancestor or diverged from each other.

Four major groups based on genome-wide polymorphism have been reported corresponding to the widely distributed species A. thaliana, A. halleri, A. lyrata and A. arenosa, and three minor groups, corresponding to the geographically limited A. croatica, A. cebennensis and A. pedemontana (Novikova et al., 2016). For three published-genome species, A. thaliana is considered as inbreeder for closely out-crossing species A. halleri and A. lyrata whose divergence from the A. thaliana is estimated to have occurred around 5 million years ago (MYA) (Ramos-Onsins et al., 2004). However, reported somewhere else, A. thaliana and A. lyrata shared an ancestor 10 MYA (Hollister et al., 2011). A. halleri and A. lyrata have around 1.5-fold larger genome than A. thaliana. Although they share more than 80% sequence identity in their genomes, there are some differences among these three species (Hu et al., 2011). A. lyrata is mainly a allogamous species whereas A. thaliana is an autogamous (Hollister et al., 2011).

One species-specific ecological trait belongs to A. halleri that is able to habit in the zones highly enriched in zinc (Zn) and cadmium (Cd) accumulating heavy metals (HM) in its aerial parts while A. lyrata and A. thaliana are both non-accumulators and sensitive to Zn and Cd (Roux et al., 2011). Despite these extremely different physiological traits, they belongs to the sister clade phylogenetically (Talke et al., 2006). Their natural distribution is also different. A. halleri is mostly seen in continental Europe, and partially in Eastern Eurasia for one of its subspecies (A. halleri ssp. gemmifera) (Roux et al., 2011). In comparison, A. lyrata is distributed in Western and Central Europe but with a circumboreal distribution. A. thaliana occurs in a worldwide manner and geographically is native of Europe and Central Asia (Al-Shehbaz and O'Kane, 2002). A study on 8 linkage groups of A. halleri revealed QTLs of rich regions of Zn tolerance (Willems et al., 2007).

A. halleri has some capacities by which it can tolerate excess of HMs and grow in the zones rich in HM. A. halleri roots are able to export metals like Cd, Zn toward its leaves (Cosio et al., 2004). This feature comes from HM ATPase HMA4 gene that has an increased copy number in A. halleri more than A. thaliana and A. lyrata (Bomblies and Weigel, 2010). Brassicaceae family show more taxa with hyperaccumulation of HMs such as Cd, Zn and Ni distributed in the species of Alyssum, Thlaspi caerulescens and A. halleri (Talke et al., 2006). In one study metallothionein 2b and 3, APX and MDAR4 in the ascorbate-glutathione pathway and certain metal transporters in P(1B)-type ATPase, ZIP, Nramp, and CDF families were overexpressed in A. halleri than in A. thaliana (Chiang et al., 2006). Previously A. halleri showed gene divergent of the 'HM-associated domain' category (Kramer, 2010; Verbruggen et al., 2009).

HMs in ionic form are highly reactive and toxic specially while being accumulated in plants as a critical agricultural problem (Olaniran et al., 2013). There are two groups of HM; essential mineral elements like Cu, Zn, Ni and Mo required in low concentrations for adequate growth and development and non-essential metals with toxic character like Cd and Pb (Arif et al., 2016). However, an excess of both groups is toxic. For example Cd can harm plants by DNA mutation, modifying protein side chains and demolishing phospholipid (Oono et al., 2014). The present study is aimed to in silico compare three genome-published Arabidopsis species including A. halleri, A. lyrata and A. thaliana. We discuss the similarities and differences among the three species in genomic level. We highlight the proteins related to HM hyperaccumulation in A. halleri as species-specific.


The reference protein, CDS (coding DNA sequences) and assembled genome files were downloaded from Phytozome (Goodstein et al., 2012) version 12 ( According to Phytozome, these files were for A. thaliana Assembly-version TAIR9, Annotation-version TAIR10; for A. lyrata Assembly-version v1, Annotation-versionv2.1 and for A. halleri Assembly-version v1 and Annotation-version v1.1. Ortho Venn was used to compare protein datasets among three species. Ortho Venn is a web-based program that can compare up to six protein datasets by clustering the input proteins of datasets and generate Venn diagram, Swiss Prot (Uni Prot) data (Poux et al., 2016) and GO enrichment for the compared datasets (Wang et al., 2015). The default parameters were employed. The SwissProt hits and protein names were compared again manually for the clusters.

Finally, the non-similar hits were studied to use for comparison of their function among three species and to extract the species-specific proteins of A. halleri. Blast + V2.7.0 (Camacho et al., 2009) was used to compare the gene models of three species using their CDS. The criteria for filtering were pident >80%, and Evalue < 1e-05. The blast-based pairwise comparisons were performed in two reciprocal directions by changing query and subject. GC content was calculated by the version 5.0.0 of the geecee program (Rice et al., 2000) in Galaxy (Blankenberg et al., 2007) for the genome and CDS of three species (

Table 1. Eleven confirmed Arabidopsis species by The Plant List in alphabetic order.

Name###Chromosome number 2n###Group

A. arenosa (L.) Lawalree###32###4

A. cebennensis (DC.) O'Kane and Al-Shehbaz###16###2

A. croatica (Schott) O'Kane and Al-Shehbaz###16###2

A. halleri (L.) O'Kane and Al-Shehbaz###16###2

A. lyrata (L.) O'Kane and Al-Shehbaz###16###2

A. neglecta (Schult.) O'Kane and Al-Shehbaz###16###2

A. pedemontana (Boiss.) O'Kane and Al-Shehbaz###16###2

A. petrogena (A.Kern.) V.I.Dorof.###16###2

A. suecica (Fr.) Norrl.###26###3

A. thaliana (L.) Heynh.###10###1

A. umezawana Kadota###16###2

Table 2. The number of clusters, proteins and singletons of three species.

Species###Proteins###Clusters###Singletons###Species clusters###Species specific clustered genes

A. thaliana###35386###22822###5766###445###1086

A. lyrata###33132###23153###6044###685###1768

A. halleri###26911###20262###4561###186###469


Table 3. The number of proteins for each comparison among three species. Species-specific proteins are sum of clustered proteins and singletons.

Comparison###Protein number###Percent of total species protein (%)

A. thaliana specific###5766+1086###19.36

A. lyrata specific###6044+1768###23.57

A. halleri specific###4561+469###18.69

A. thaliana _ A. lyrata###7850###A. thaliana 22.18

###A. lyrata 23.69

A. thaliana _ A. halleri###2328###A. thaliana 6.58

###A. halleri 8.65

A. halleri _ A. lyrata###2591###A. halleri 9.63

###A. lyrata 7.82

A. halleri _ A. lyrata _ A. thaliana###62966###66

Table 4. Transcript (CDS) pairwise comparisons of three Arabidopsis species.

Query###A. halleri###A. lyrata###A. thaliana


A. halleri###-###27121 (81.8%)###30228 (85.4%)

A. lyrata###24854 (92%)###-###32483 (91.8%)

A. thaliana###24246 (90.1%)###28756 (86.8%)###-

Table 5. GC content and number of base pairs for 3 Arabidopsis species.

Species###GC content (genome)###Genome size (bp)###GC content (CDS)###CDS size (bp)

A. halleri###37.05###127615339###43.74###31383222

A. lyrata###37.74###206667935###44.62###38615903

A. thaliana###36###119667750 (119146348)###44.40###43546761

Table 6. The species-specific genes of A. halleri related to HM response.

Protein###SwissProt hit###HM###Function###Reference

Araha.10286s0004.2.p###oligopeptide transporter###Al, Cd###Transport,###(Patel 2007; Chen et

Araha.10286s0004.1.p###phytochelatin###al., 2017)

Araha.3113s0004.2.p###putative purine permease###Al###Transport###(Chen et al., 2017)


Araha.11872s0001.5.p###Aldehyde dehydrogenase family###Al, Cd###Detoxification###(Chen et al., 2017)

Araha.11872s0001.1.p###2-member C4 Q56YU0





Araha.7027s0001.1.p###Cellulose synthase-like protein###Al, Cd###Cell wall###(Song et al., 2013;

Araha.7027s0001.2.p###O23386###Chen et al., 2017)

Araha.32714s0001.4.p###Importin subunit alpha-1 Q96321###Al, Cu,###Transport###(Chen et al.,, 2017;

Araha.32714s0001.3.p###Si###Jang et al., 2018; Wang

###et al.,, 2017)

Araha.23960s0001.1.p###Cysteine synthase 1 P47998###Cd, Zn###Detoxification###(Kawashima et al.,

Araha.23960s0001.2.p###2004; Kim et al., 2011;

###Konlechner et al.,


Araha.0018s0018.1.p###Plasmodesmata callose-binding###Al###Transport###(Chen et al., 2017)

Araha.0018s0018.2.p###protein Q9M2K6


Araha.7955s0008.4.p###Probable BOI-related E3###Al###Degradation,###(Chen et al., 2017)

Araha.7955s0008.2.p###ubiquitin-protein ligase 3


Araha.51292s0001.1.p###SNF1-related protein kinase###Al, Cd###Signaling, ROS###(Kulik et al., 2012;

Araha.51292s0001.2.p###catalytic subunit alpha KIN11###Chen et al., 2017)


Araha.8372s0003.1.p###Translocase Q9SLF3###Al, Cd###Transport###(Chen et al., 2017)



Protein clusters and singletons: The proteins of three species formed 24816 clusters, 23500 orthologous clusters (at least contains two species), 1316 species-specific cluster sand 16371 singletons (those were not clustered and are unique to the species) (Figure 1 and Table-2). Although the genome of A. thaliana is smaller than two other species but its protein number is bigger likely due to better assembly and availability of data for A. thaliana. A. halleri shows less singletons, clusters, and unique proteins maybe because of its lower number of proteins compared to the other two. The common clusters were 17921 containing 62966 genes among all three species while pairwise common proteins between two species were 12769 distributed in 4733 clusters (Figure 1 and Table 3). Three species showed 66% common proteins. The more pairwise common proteins were seen between A. thaliana and A. lyrata with 22-23% for each species. The least belongs to A. thaliana while compared with A. halleri with 6.58%.

These results are not in accordance with the chromosome number groups as it is expected that A. halleri and A. lyrata belongs to the same group and A. thaliana is diverged differently from them in another single species group. This might be due to the lower proteins reported for A. halleri and better annotation and assembly for A. thaliana and A. lyrata. A. lyrata showed the most species-specific proteins including clustered and singletons. The analyses about singletons for three species will be reported in further studies.

Gene comparison: The blast-based pairwise comparisons of CDS showed that there is at least more than 81% similarity among all three Arabidopsis species in general. Interestingly, the most similarity exist between A. halleri (query) and A. lyrata (subject) and the least between A. lyrata (query) and A. halleri (subject) (Error! Not a valid bookmark self-reference.). A. halleri showed more similarity with the two other species when it is query but when it is subject the least similarities seen. These results might be due to this fact that blast is based on the number of the genes in the database and there are less genes for A. halleri. The blast outputs when A. halleri is subject are similar to the outputs generated by Ortho Venn. These results are in accordance with the results obtained for protein clusters.

Because of its influence on CpG islands, DNA methylation, DNA stability, exon length and transcription, it plays a vital role in gene and genome regulation (Singh et al., 2016; Tirado-Magallanes et al., 2017). It determines the physical properties of the genome. It provides a vision on how genome/chromosome size can be among different species, genera, towards kingdom (Li and Du, 2014). GC content has been reported 36% for genome of A. thaliana (Meister, 2005) and its ESTs (Shangguan et al., 2013) that is in accordance with our results taking into account that we have used the most recently assembled genome. However, A. lyrata and A. halleri showed very close GC content that is more than that of A. thaliana. This suggests that they might be closer in terms of GC/AT domains (Error! Not a valid bookmark self-reference.). GC content of transcriptome show very close similarities among three species suggesting similar transcription pattern among them.

Our results of GC content for transcripts are similar to the GC levels of coding sequences of Oryza sativa (43.6%), Glycine max (45%) and A. thaliana (44%) (Severin et al., 2010; Smarda et al., 2012). Interestingly, CDS size is not in coherent with genome size and the biggest one belongs to A. thaliana with the smallest genome. This might be due to high copy number of genes in A. thaliana although its genome size and chromosome number is less than the other two species. This needs further studies to reveal how they have diverged from their common ancestor and which evolutionary events have occurred.

Genes related to resistance or response to HMs: Interestingly, among the different genes, those are species-specific for A. halleri, there are the 26 genes from 10 clusters related to HM (like Cd, Al, As and Zn) resistance and response. They belong to genes with different functions like transporter, different detoxifying enzymes, signaling and regulation (Error! Not a valid bookmark self-reference.). These genes have been reported to be involved in HM response and tolerance in plants (DalCorso et al., 2010). Most of these genes reported by Chen et al., are differentially expressed in Fagopyrum esculentum Moench functioning in resistance and response to aluminum (Al) (Chen et al., 2017). Meantime, they are related to other HM responses in plants as well.

The genes with GO terms related to Zn and Cd compared. The findings show that A. halleri possess the enzyme "Cysteine synthase 1" under GO term response to Cd as species-specific term (Kawashima et al., 2004; Kim et al., 2011). In plants resistant to Cd stress cysteine is synthesized in order to regulate glutathione GSH biosynthesis. Then GSH a non-protein thiol acts as an antioxidant to detoxification of Cd (Gill and Tuteja, 2011). On the other hand, sulfur (S) and Cd show a direct relation as uptake and assimilation of S can determine Cd resistance in crops via cysteine synthesis targeting GSH. A. halleri possesses two proteins of Cysteine synthase. Oligopeptide transport (OPT) gene family of integral membrane proteins is involved in diverse functions like long-distance sulfur distribution, nitrogen mobilization, metal homeostasis, and HM sequestration through GSH transport, metal-chelates, and peptides (Lubkowitz, 2011).

In addition, phytochelatins/metal chelats are synthesized in plants resistant to Cd as a part of detoxification (Gill and Tuteja, 2011). It is proved that overexpression of OPT causes Cd hypersensitivity and accumulation in A. thaliana roots (Mendoza-Cozatl et al., 2014). A. halleri has two species-specific members of OPT those can make it tolerant to HM and may facilitate Cd hyperaccumulation in A. halleri. Oxidation of toxic aldehydes to carboxylic acids is of functions of ALDHs those belong to a family of NAD(P) + -dependent enzymes. They are highly expressed in response to drought, salinity, water excess, oxidative stress and HMs (Jimenez-Lopez et al., 2016). ALDH2 has been reported that function in Al stress (Singh et al., 2013). ALDH can function via decreasing accumulation of lipid peroxidation-derived reactive aldehydes as a detoxification pathway to increase tolerance in plants (Sunkar et al., 2003).

We found 6 ALDHs in A. halleri those may function similarly in response to HM. Sedum alfredii Hance hyperaccumulating ecotype has shown constitutively upregulation of cellulose synthase gene while being exposed to Cd (Gao et al., 2013). In Elsholtzia splendens, a hyperaccumulator of Cu, the composition and distribution of root cell wall and cellulose was altered in excess of Cu that can improve cellulose, hemicellulose and pectin contents during HM exposure (Le Gall et al., 2015). In a low-Cd mutant of rice, a correlation between cellulose synthase subunit 9 and Cd accumulation in roots, leaves, grains and altered vascular structure have been reported. This mutation of CESA9 (E101K) affects Cd transport efficiency targeting low Cd accumulation by altering cell-wall properties in the conducting tissues (Song et al., 2013). However, cell wall and xylem alteration are involved in HM tolerance mechanisms by preventing HM translocation or deposition (Vollenweider et al., 2006).

Two copies of cellulose synthase are found in A. halleri. Importin is involved in nuclear import and export processes transporting other proteins intro nucleus by binding to nuclear localization signal (NLS) motifs (Tran et al., 2014). It has two subunits; [alpha] and [beta]. Importin [alpha] binds to NLS and [beta] binds to molecules transporting them to the nucleus. A C2-domain-like protein with NLS motif is highly expressed in response to different HMs in barley (Ouelhadj et al., 2006). In response to Cu and Si, importin [alpha]is induced and can act with NLS (Wang et al., 2017; Jang et al., 2018). In A. halleri with these two proteins, it may play a similar role in binding to such motif to tolerate HM excess. When plants are exposed to HM (Al, Cd, Cu etc.), they accumulate callose at plasmodesmata causing alteration in their permeability (De Storme and Geelen, 2014). This then regulate heavy metal transport via plasmodesmata (O'Lexy, 2017).

In order to activate such permeability, plasmodesmata callose-binding protein plays a role by interacting with other transporters like CTL1 (Gao et al., 2017) in vesicle trafficking. This protein can manage metal transport and function in metallic ion channels (Gao et al., 2017). They may facilitate channels from which HM can import and export to root cells toward leaves. Three clustered proteins of plasmodesmata callose-binding protein suggest the existence of similar mechanism for A. halleri. Ubiquitination pathway is one of the ways whose participation in plant abiotic stress tolerance has been proved (Dametto et al., 2015). Protein degradation by the ubiquitin/proteasome 26S system plays an important role in HM stress response via removing damaged proteins (Dametto et al., 2015).

BOI-related E3 ubiquitin-protein ligase 3 as an E3 ubiquitin-protein ligase functioning in ubiquitination has been reported that is involved in the regulation of pathogen and abiotic stress responses by facilitating degradation of MYB108/BOI (Luo et al., 2010). One OSHIR1 (E3 ubiquitin-protein ligase) is involved in As and Cd uptake (Hasan et al., 2017) by interacting with OsTIP4;1 a tonoplast intrinsic protein in the plasma membrane. This degradation and regulatory function may occur in A. halleri by three discovered proteins. SNF1-related protein kinase catalytic subunit alpha KIN11 belongs to the SNF1-related protein kinase family that is involved in many biological processes like signaling cascade, senescence, transcriptional and post transcriptional regulatory, phosphorylation of enzymes involved in various pathways (Crozet et al., 2014; Wang, 2017). SnRK KIN11 control convergent reprogramming to darkness, sugar level and stress (Kulik et al., 2011).

One of this family SnRK2 functions in Cd resistance by regulating ROS accumulation in plant root (Kulik et al., 2012). By employing these two disclosed proteins, A. halleri might follow the similar pattern. Translocase is one protein located in inner and outer membrane of mitochondrion. It mediates transport of proteins from nuclear coding genes in mitochondrion. Its expression has increased in ROS scavenging in response to Cd (Yu et al., 2017) and Al (Chen et al., 2017). However, its exact role is not clear yet. Phytochelatins, phytohormones like ABA, BR, SA and transporters are crosstalk elements in diverse plant stresses that are also involved in HM stress (Nunez Vazquez et al., 2013). HM responsive genes share similar function as they employ almost identical mechanisms to respond to other abiotic stresses like osmotic, oxidative, drought, salinity, as well as biotic stress (Chinnusamy et al., 2004; Zhu, 2016).

As there exist diverse stresses at the same time surrounding plants, these crosstalk and common responsive genes can collaborate to mitigate the impacts of stresses on plants (Chinnusamy et al., 2004). It can be worthy then to study different stresses at the same time to understand how different stresses (HM and osmotic stress for example) can share alike responses and genes (Jazayeri, 2015).

Conclusions: The findings disclosed that in species level there are around 10-20% difference among three Arabidopsis species taking into account the criteria for similarity. Speciation might count on such differences that we can see among close species of a genus. Interestingly, A. halleri has a genetically physiological speciation character different from two other species; i.e. resistance to HMs. The findings imply that A. halleri has acquired the built-in mechanism to tolerate and detoxify HMs during speciation process and evolutionary events. A. halleri is naturally hyperaccumulator of HMs like Zn and Cd and hypertolerant to HMs while two other species are not tolerant. However, the function in resistance process in Arabidopsis needs further expressional and functional analyses to disclose the role of the presented genes in HM detoxification and accumulation. HM stress as an abiotic stress can share common mechanisms causing tolerance in plants.

Signaling network, functional enzymes and regulatory system are involved in several stress response in plants. We hypothesize that oxidative, osmotic, drought and salinity stress responses in plants can make networks of coexpressing genes by which plants control diverse environmental factors and ecological impacts. Further studies are required to disclose common responses among abiotic stress with HMs.


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Publication:Journal of Animal and Plant Sciences
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