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Flax Lectin Gene Expression
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This entry is adapted from the peer-reviewed paper 10.3390/plants11020163

Plant proteins with lectin domains play an essential role in plant immunity modulation, but among a plurality of lectins recruited by plants, only a few members have been functionally characterized. The lectin gene expression in flax root tips infected with Fusarium oxysporum was analyzed. For the analysis of flax lectin gene expression, FIBexDB was used, which includes an efficient algorithm for flax gene expression analysis combining gene clustering and coexpression network analysis. Two pools of lectin genes have been revealed: downregulated and upregulated during the infection. 

flax (Linum usitatissimum) Fusarium oxysporum gene expression plant lectins

1. Introduction

It is generally accepted that lectins are proteins capable of recognizing and binding specifically and reversibly to carbohydrate structures without changing the carbohydrate moiety. Initially, lectins were discovered as highly toxic molecules, and their protective function in plant life was considered to be directly entomotoxic [1]. Following the discovery of non-toxic lectins, a better understanding of the role of proteins with lectin domains in plant defense and symbiotic interactions has emerged; such participation occurs via signaling pathways which are associated with microbe- or pathogen-associated molecular patterns (PAMP and MAMP) [2][3]. At the same time, involvement of plant lectins in cell organization, embryo morphogenesis, phagocytosis, growth mechanisms of cells, induced mitosis, pollinic recognition, and active engagement in the transport of carbohydrates and their establishment in plant tissues has been demonstrated [4].
Plant proteins with lectin domains are divided into 12–18 families in accordance with their conserved carbohydrate-binding sites, the sequence, and the three-dimensional structure of the lectin motif [5][6][7]. The majority of the families are named after their most studied representative within the group, for example, GNA (Galanthus nivalis agglutinin), Legume (first described for Leguminosae), Malectin and Malectin-like (maltose and related oligosaccharide binding lectin), LysM (Lysin motif), Nictaba (Nicotiana tabacum agglutinin), Calreticulin (calcium-binding protein present in the endoplasmic reticulum), etc. [6]. Analysis of fully sequenced plant genomes revealed a huge variety of plant lectins, both quantitative and qualitative. An important feature of plant lectins is the presence of repeated combinations of certain protein domains, such as the GNA, Legume, LysM, Malectin, and Malectin-like domains, along with a protein kinase domain. Such chimeric proteins form an extensive group of lectin receptor-like kinases (LecRLK), which are part of the plant immune system [8].
Recently, the revision of flax (Linum usitatissimum L.) proteins with lectin domains has been carried out [6]; 406 genes encoding lectin domain-containing proteins in the flax genome were identified. In the current work, we consider flax lectins via the prism of their “classic” function (as defense proteins) and analyze the behavior of flax lectins in root tips during fungal infection. The transcriptomic data for different flax cultivars’ root tips, which reflected the early response of flax plants to Fusarium oxysporum action [9], was integrated into the FIBexDB [10], and we were able to assess the response of stage-specific genes encoding proteins with lectin domains in the case of Fusarium wilt of flax plants and compare them to samples attributed to stem tissues of plants grown under normal conditions. The searchers' findings shed new light on the role of lectins in plant defense and development in general, as well as on the potential functions of specific proteins with lectin domains.

2. Expression of Flax Genes for Lectins during Fungal Infection in Different Cultivars

In flax root tips, 304 genes with lectin domains were expressed (threshold of TGR (total gene read) value ≥ 16 at least in one sample). According to the cluster analysis performed using FIBexDB, this set of lectin genes was subdivided into three clusters (Figure 1): 63 genes accounted for the cluster where genes in general showed down-regulation of expression in the root samples of all flax genotypes treated with F. oxysporum compared to controls (cluster 1). The expression of 216 genes was upregulated in all flax genotypes treated with F. oxysporum as compared to controls: 146 genes were upregulated in all infected plants independently of the flax genotype (cluster 2). Cluster 3 included 70 genes whose expression in the susceptible cultivars was less pronounced compared to the resistant cultivars and hybrids.

Figure 1. (a) Cluster analysis of 304 genes expressed in flax root tips of different genotypes treated with Fusarium oxysporum. A heatmap was built in FiBexDB. CTR1,2,3,4,(1x3),(1x4)—untreated root tips of different flax genotypes, FOX1,2,3,4,(1x3),(1x4)—root tips of different flax genotypes treated with F. oxysporum. *—genes for lectins upregulated in cultivars resistant to F. oxysporum. (b) Members of different lectin gene families in the analyzed clusters. Red arrows mark family members which were abundant in the analyzed clusters.

3. Genes Encoding Lectins Potentially Involved in the Biosynthesis of Cell Compounds

During the analysis of the lectin gene expression in different flax tissues and organs, the expression of 85% of lectin genes was detected in all analyzed tissues, but at different levels. About 20% of the lectin genes expressed in the root tips were downregulated during the fungal infection. Genes belonging to the Calreticulin and Galactose-binding lectin (Gal_lectin) families were enriched in the cluster of genes downregulated during the infection. Among the genes initially with a high level of expression were those encoding calreticulins. Arabidopsis calreticulins (CRTs) and calnexins (CNXs) are known as the glucose-binding lectins [8], involved in the folding and subunit assembly of the majority of the Asn-linked glycoproteins [11]. CRTs were referred to as the proteins involved in the folding of other proteins [12] with stable gene expression levels in all analyzed flax tissues [6]. Their downregulation in the course of the infection, when all general biosynthetic processes are suppressed, is reasonable. Moreover, it was shown that the loss of function of CRT1a (AT1G56340) reduces plant susceptibility to the fungal pathogen Verticillium longisporum in both Arabidopsis thaliana and Brassica napus [13] and results in activation of the ethylene signaling pathway, which may contribute to the reduced susceptibility.
Under osmotic or other abiotic stresses, CNX showed a highly reducible accumulation in the developing soybean roots [14], but a negative correlation between the calreticulin gene expression and the defense reaction development to the fungal infection was not reported. A similar dynamics of the CRT expression was observed in gravistimulated flax tissues. It was shown that the transcripts coding for calreticulin and calmodulin were recruited into polyribosomes predominantly in the lower half of gravistimulated maize pulvini [15]. Obviously, intensive protein biosynthesis and related processes of protein folding control with the involvement of calreticulins are inherent in flax root tips (close to the root apical meristem), shoot apical meristem, and gravistimulated stem tissues, and are suppressed in the course of stress reactions caused by fungi.
Most of the lectin genes referred to as potentially associated with the primary cell wall development [6] were suppressed during the fungal infection. Among the genes encoding proteins with lectin domains drastically downregulated during the infection in all flax genotypes, the BGAL genes were widely presented. Such associations can be related to the modifications of pectin or other hemicelluloses that compose the primary cell wall. For example, xyloglucan was determined as a substrate for Arabidopsis BGAL10. This BGAL activity was required for the structural features of xyloglucan, which in turn provided a suitable environment for interaction with cellulose microfibrils during the primary cell wall extension in young tissues [16]. Though LusBGAL3 was predicted as an extracellular protein, it was closely coexpressed with the genes encoding enzymes involved in pectin biosynthesis: galacturonosyltransferases (GAUTs) and (SAM)-dependent methyltransferases (SAM_Metases). SAM_Metases catalyze the transfer of a methyl group to an acceptor molecule. This family of plant methyltransferases contains enzymes that act on a variety of substrates, including salicylic acid (SA), jasmonic acid (JA), and 7-methylxanthine [17]. Involvement of a putative Arabidopsis S-adenosyl-L-methionine (SAM)-dependent methyltransferase, termed QUASIMODO 3 (QUA3, At4g00740), in methylesterification of the pectin homogalacturonan (HG) was supposed [18]. Flax ortholog of AtQUA3 (Lus10000808) was presented in the coexpression network of LusCNX1; Lus10037101 (homolog of AT1G13860, encoding QUASIMODO2 LIKE 1) was found in the coexpression network for LusBGAL3. The degree of methylesterification of pectin affects the adhesive properties of pectin [19]. The association of LusBGAL gene expression and HG biosynthesis is probably not direct, but we can assume that BGALs with lectin domains are closely associated with the primary cell wall biosynthesis, which is suppressed during fungal infection.
During the infection, the expression of genes encoding malectins with an additional kinesin domain was downregulated. According to the list of coexpressed genes, these malectins are involved in the microtubule cytoskeleton organization. The orthologous gene in Arabidopsis At2g22610 encodes kinesin MDKIN2, which, as was suggested, may be related to its cargo or protein binding ability and has diverged functions at different points in the cell cycle and in different subcellular locations. GUS staining for MDKIN2 revealed expression in diverse plant tissues but predominantly in the vasculature and dividing tissues such as growing leaves and root tips [20]. It is suggested that if the MDKIN2 malectin domain can similarly bind to polysaccharides, its localization during cytokinesis may indicate a function in the organization of cell wall components [20]. This assumption is supported by the revealed coexpression with the flax malectin gene (Lus10035954) of the gene encoding CSLD5.1 (Lus10010024, ortholog of AT1G02730). For CSLD5, the expression has been shown to be cell cycle dependent and appears to be involved in the phragmoplast formation in Arabidopsis [21].

4. The Avant-Garde of Defense Flax Lectins in Response to Fusarium oxysporum

Absolute champions among genes whose expression was significantly upregulated in the flax root tips during the fungal infection were those belonging to the Hevein and CRA families: the level of expression increased a hundred times compared to the control samples. These proteins possess a chitin-binding domain along with chitinase activity and cannot be considered as “true” lectins [22]. For the Hevein-like antimicrobial peptides, binding to chitin is supposed to be vital for their antifungal activity, although the exact mechanism of their action remains unknown [23]. Activation of the oxidative and reductive processes during the infection is a common reaction in plants and there are plenty of known participants, including cytochromes p450 and short-chain dehydrogenase/reductases [24]. In plants, cytochromes P450 are closely related to the biosynthesis of phytoalexins [25]. In total, 31 genes for the cytochrome p450 superfamily belong to the following different families: CYP71, CYP76, CYP81, CYP82, CYP84 (all of them are in clan CYP71 [25]) coexpressed with Lus10028377 (r > 0.95). Fifteen SDR genes (short-chain dehydrogenase/reductase (SDR) family protein, SDR2 and SDR5) were found to be coexpressed with Lus10028377 (coefficient of coexpression r > 0.94). We can assume that different members of the cytochrome p450 superfamily and SDR act on different steps of diterpene phytoalexin metabolism, as was shown for rice [26], but whether chitinases are directly involved in this process remains unknown. It was shown that chitin oligosaccharides from the fungal cell walls induce the momilactone cluster genes in rice, one of two gene clusters involved in the biosynthesis of rice diterpene phytoalexins [26].
Among the lectins whose gene expression was upregulated under the Fusarium infection, proteins with the Nictaba domain were present. The first carbohydrate-binding protein with the Nictaba domain was observed in the leaves of Nicotiana tabacum plants after treatment with jasmonates or insect herbivory [27]. Later, the interaction of the Nictaba lectin with different core histones was shown within the nucleus of the plant cell through their O-GlcNAc modification [28]. Interestingly, all of the Nictaba genes were found to be coexpressed with the Lus10039911 gene, which encodes JASMONATE-ZIM-DOMAIN PROTEIN 1 (JAZ1) and a number of genes for WRKY transcription factors (WRKY40, 41, 33, and 26). It was shown that some members of WRKY (WRKY40, 57, and 75) are able to activate expression of the JAZ genes, which are known as JA-induced repressors of the JA signaling pathway [29][30][31]. The WRKY transcription factors are widely known for their vital role in the plant’s response to both external and internal stimuli, including the response to the fungal pathogen F. oxysporum [32]. It was shown that WRKY33 may function as a downstream component of the MPK4-mediated signaling pathway and contribute to the repression of SA-dependent disease resistance [33]. Specific upregulation of the Nictaba genes in the root tips and mature xylem under normal conditions gives us reason to suggest that flax Nictaba genes for proteins with F-box domains (Lus10015208, Lus10015209, Lus10031473, Lus10031471, all homologous to At1G56250), are specifically expressed in the vascular system. For Arabidopsis plants, it was shown that the At1G56250 gene product is a VBF (VIP1-binding F-box) protein. VBF expression is known to be induced by Agrobacterium and facilitate tumor formation, suggesting that the host factors that the pathogen uses for infection also include those that the plant initially produces to defend itself from the very same infection [34].
Xylem tissue is at the “forefront” of fungal attack: after penetration of the root epidermis, hyphae progress intercellularly via the root cortical cells until they enter the xylem tissue, where wilt processes develop [35]. In this case, it could be reasonable to suggest that developing xylem tissue in the root tips accumulates quite a number of defense proteins, including lectins and other substances, in order to be ready in advance to face the possibility of a pathogen attack. We can assume that the xylem-specific lectins are more likely to be involved in the defense processes and modification of various substrates than in biosynthetic processes.
Some genes encoding defense proteins, including lectins, have a definite level of expression in the tissues under normal conditions. A pathogen attack increases the transcript abundance, while the expression of a number of genes is strongly induced during the infection. Lus10000579, encoding a GNA family member, had a high level of expression in the root tips and increased it during the infection; it is a homolog to AT1g78850 (AtGAL1), which encodes a curculin-like (mannose-binding) protein. It was shown that the Arabidopsis cells in a suspension culture accumulate this lectin as well as endochitinase AT3g12500 (homolog for Lus10028377, which was described above) in response to a chitosan elicitor in the cell wall fraction [36]. Under normal conditions, Lus10000579 had the highest level of expression in hypocotyls and root tips; this gene probably plays an important role in the early stages of development, being susceptible to fungal infection.

5. Lectins That Might Determine the Resistance of Flax to F. oxysporum

In the course of clusterization of the flax lectin genes in different stem tissues and root samples, a group of lectin genes whose expression differed in the susceptible and resistant flax cultivars was revealed. The genes encoding amaranthins (Lus10005395 (LuALL3), and Lus10005397 (LuALL2)) had the highest level of expression in all flax genotypes, even in the control samples, and were upregulated under the fungal infection, this upregulation being more pronounced for the resistant cultivars and their hybrids. Transcripts of both these genes significantly increased in abundance in the etiolated flax seedlings following the methyl jasmonate (MeJA) treatment, but not by SA [37]. In the root tips and seedlings, the LuALL2 and LuALL3 transcripts were generally abundant in untreated tissues as well [37]. It was shown that the signaling pathway of the initially anti-stress plant hormone MeJA plays both a positive and a negative role in the resistance of A. thaliana to F. oxysporum. This is due to the fact that pathogens reprogram the physiological functions of the host to increase susceptibility to infection [38]. Indeed, Lus10004990 (homolog of AT4G36920) encoding an ethylene responsive APETALA2 (AP2)-domain transcription factor being also a jasmonate-responsive gene [39] was upregulated in the infected root samples and activation in the resistant cultivars was more pronounced (data not shown). Interestingly, flax has one of the largest families of amaranthin-like lectins among other plant species [37]. Many taxonomically distant plant species, including Arabidopsis, do not have amaranthin-like lectins in their genomes [6][40].
We found that amaranthin genes were in coexpression with 1-DEOXY-D-XYLULOSE 5-PHOSPHATE SYNTHASE 1 (DXS1). The DXS1 is associated with the production of terpenoids (MEP (non-mevalonate) pathway) [41][42]. It has been shown that in flax, the non-mevalonate pathway is strongly activated at the beginning of the F. oxysporum infection and a redirection of metabolites towards abscisic acid (ABA) synthesis takes place [43].
The hypothetical involvement of proteins with lectin domains in plant defense is summarized in Figure 2.
Plants 11 00163 g007 550
Figure 2. The hypothetical involvement of proteins with lectin domains in plant defense. The lectin gene whose expression changed drastically during the Fusarium oxysporum infection and their potential association with the general processes are presented. The downregulated and upregulated pathways are given in blue and red backgrounds, respectively. Lectins are part of a comprehensive network of plant-pathogen interactions that includes cross-talk between plant resistance and pathogen spread. SA—salicylic acid, JA—jasmonic acid, ABA—abscisic acid, MEP—non-mevalonate pathway.

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