Plant annexins: Structural diversity, evolution, and multifunctional roles in development and stress tolerance

Introduction

Annexins are an evolutionarily conserved multigene family of Ca 2+ -dependent, phospholipidbinding proteins (Tong et al., 2025) [46] found in prokaryotes, fungi, plants and animals (Mortimer et al., 2008; Huh et al., 2010) [36,23] . Significant homology between eukaryotic annexins and alpha-giardin proteins of unicellular protozoan Giardia lamblia evidence annexins existence back ~1-1.5 billion years ago (Morgan and Fernandez, 1995) [35] . The annexins superfamily has been classified into annexins in vertebrates (A family), in invertebrates (B family), in fungi and few unicellular eukaryote groups (C family), in plants (D family), and in protists (E family). Additional gene subfamilies have been emerged as a result of extensive and independent lineage-specific gene (or) genome duplication which is evident through their molecular phylogeny, gene structure and chromosomal distribution (Warmus et al., 2026, Moss and Morgan, 2004) [48,37] . Annexins are abundant in plants representing 0.1% of their total cell protein and resemble animal annexins in size and activities. Partial peptide sequences of annexin proteins precipitated in the presence of Ca 2+ and phosphatidylserine in tomato, corn and lily showed homology to sequences found in animal annexins (Davies, 2014) [10] .

Structural features

Structurally, all annexins have a common core domain made up of four identical domains/repeats of ~ 70 amino acids long. Each domain/repeat is made up of five short α helices which are wound into a right-handed super-helix and contains a characteristic type II motif (conserved endonexin sequence of GxGT-(38 residues)-D/E) for binding calcium ions (Shail and Prasad, 2022) [42] . These α helices are joined together by short loops, which are essential for Ca 2+ -annexin interactions (Laohavisit and Davis, 2011) [31] . Annexins also contain a variable long amino-terminal region with sites for post translation modifications and interaction with other proteins (Yan et al., 2026 Moss and Morgan, 2004) [51,37] .

Annexin resembles a flattened disc like structure on which Ca 2+ binding motifs are located towards convex surface and amino and carboxyl termini towards concave surface. In plant annexins, characteristic type II motif for binding calcium ions present in the first and fourth repeats only (Moss and Morgan, 2004; Jami et al., 2012) [37,24] . Recent biochemical analysis and three-dimensional crystal structure studies shown that plant annexins exhibit Ca 2+ dependent phospholipid membrane binding via domain I and IV (Hofmann et al., 2000, 2003; Hu et al., 2008) [20,19,22] . Plant annexins also contain short amino-terminal region (~10 amino acids) which have the sites for post-translational modifications and protein-protein interactions. This aminoterminal tail is thought to be the regulatory domain which may confer specific functions upon each annexin member (Liemann and Huber, 1997) [34] . Lack of long aminoterminal region and predicted calcium binding sites in their second and third domains made up plant annexins a monophyletic cluster in contrast to annexins of vertebrates (Moss and Morgan, 2004; Jami et al., 2012) [37,24] . Presence of motifs responsible for calcium channel and actin binding activity as well as peroxidase and ATPase/GTPase activity in plant annexins has been confirmed through sequence analysis (Mortimer et al., 2008) [36] .

Annexins in plants

Annexins are abundant cellular proteins found mainly in cytoplasm, cell organelles (nucleus, Golgi apparatus, chloroplast) and in the membrane system (ER, secretory vesicles, plasma membrane) and are suggested to play a role in wide variety of essential cellular processes (Yan et al., 2016) [50] . Though plant annexins were first identified, thirty years ago in tomato (Boustead et al., 1989) [3] , only limited information of annexin gene families is available till now and so far only Arabidopsis thaliana and Brassica juncea annexin gene families have been well characterized (Clark et al., 2001; Cantero et al., 2006; Jami et al., 2009) [6,4,26] . Available whole genome sequences of various plant species in the public databases provided an opportunity for detailed molecular, evolutionary and functional studies in annexin gene families. With the available whole genome sequences, eight annexin genes in Arabidopsis (Clark et al., 2001) [6] and ten annexin genes in Oryza (Jami et al., 2012) [24] were identified. Jami et al. (2012) [24] performed a genome-wide survey of annexin multigene families in 16 plant species ranging from unicellular green algae to multicellular plants, and identified 149 annexins. All the 149 deduced protein sequences further classified into nine arbitrary groups of related protein clades. Presence or absence of predicted calcium binding sites (CBS) in the core domains/repeats indicated the different calcium binding specificities of plant annexins in the nine groups. Comparative sequence analyses in 149 plant annexins through PROMALS3D for conservation of amino acid residues revealed presence of two Glycine residues, IRI-motif, DXXG-motif and histidine residue in annexin domains which are thought to be essential for ion channel activity, phosphodiesterase activity, peroxidise activityand secondary structure maintenance of annexin proteins (Jami et al., 2012) [24] . The rice annexin Os05g31760 contains two RGD motifs and a Cysteine-rich and a zinc finger type (C2H2) domain that are thought to be involved in cell attachment and transcriptional regulation (Jami et al., 2012) [24] .

Expression and Localization

Annexin genes are expressed in most of the plant tissues and organs at different developmental stages throughout the life cycle (Mortimer et al., 2008) [36] . Delmer and Potika (1997) [12] observed high level of expression of AnnGh1 and AnnGh2 proteins in all major tissue of cotton by using polyclonal antibodies that recognizes annexin proteins. Several immunological studies showed higher expression of annexin proteins in cells actively involved in secretion or fruit ripening (Blackbourn and Battey, 1993; Clark et al., 1992, 1994; Proust et al., 1996) [2,8,39] . Enhanced tissue specific expression of annexin proteins during the process of fruit ripening was reported in strawberry (Wilkinson et al., 1995) [49] and pepper (Proust et al., 1996) [39] . Similarly, tissuespecific expression of several annexing gene families was observed in Arabidopsis (Lee et al., 2004) [33] , Mimosa (Hoshino et al., 2004) [21] , Capsicum (Hofmann et al., 2000) [20] , Zea mays (Caroll et al., 1998) [5] etc. Differential expression has been noted during the cell cycle in tobacco (Proust et al., 1999) [40] , embryogenesis in Medicago (Gallardo et al., 2003) [14] , pollen and seed germination in Oryza sativa (Dai et al., 2006; Yang et al., 2007) [9,52] , tuber enlargement in Manihot esculenta (Sheffield et al., 2006) [43] , fiber development and elongation in Gossypium (Shin and Brown, 1999; Yang et al., 2008) [44,53] and lateral root development in Medicago (de Carvalho-Niebel et al., 2002) [11] .

Plant annexins in stress response

Expression of plant annexin genes is found to be regulated by various biotic and abiotic stress factors and stress inducers. Since after the first report by Kovacs et al. (1998) [30] in alfalfa, regulation of plant annexin genes by different stress conditions (drought, salinity, cold, heat, heavy metal and oxidative stress) and/or by different phytohormones (ABA, Jasmonic acid, ethylene, SA and auxin) has been reported in Arabidopsis (Lee et al., 2004 [7,1] , Brassica (Jami et al., 2008, 2009) [24,25] , rice (Gorantla et al., 2005; Jami et al., 2012) [17,24] and turnip (Yan et al., 2016) [50] . Genetic transformation approaches have shown that annexins play a significant role in protecting plants from both biotic and abiotic stresses (Lee et al., 2004 [33,24,29,13,23,54] . For example, ectopic expression of Indian mustard annexin gene (AnnBj1) in tobacco (Jami et al., 2008) [24] and in cotton (Divya et al., 2010) [13] provided enhanced tolerance to various abiotic stresses such as salinity, dehydration, oxidative stress and heavy metal stress during seedling growth and development. Transgenic potato plants ectopically expressing StAnn1 have shown more efficient protection of reaction centers of photosystem II (PSII) and higher accumulation of chlorophyll b and xanthophylls than WT plants under drought conditions (Szalonek et al., 2015) [45] . Over expression of a cotton annexin gene, GhAnn1, contributed to increased salt and drought stress tolerance in transgenic cotton plants (Zhang et al., 2015) [54] . AnnAt1overexpressing mutants in Arabidopsis showed drought tolerance, while loss-of-function mutants were drought sensitive (Konopka-Postupolska et al., 2009) [29] . Over expression of annexin gene, CkAnn in transgenic cotton caused a significant increase in drought tolerance and enhanced disease resistance to Fusarium oxysporum (Zhang et al., 2011) [55] .

Annexins in oxidative stress tolerance

Plant annexins from M. sativa and A. thaliana have been implicated in oxidative stress response. In particular it has been shown that an annexin like protein from Arabidopsis, is able to rescue Escherichia coli ∆ OxyR mutants from H 2 O 2 stress (Gidrol et al., 1996) [16] . It has also been shown that an Arabidopsis annexin, AnnAt1 also possess peroxidase activity (Gorecka et al., 2005) [18] . More recently annexins of maize, Indian mustard, capsicum, cotton were also shown to exhibit peroxidase activity (Mortimer et al., 2008; Jami et al., 2008; Laohavisit et al., 2009; Zhang et al., 2015) [36,24,32,54] . The peroxidase activity of annexins is due to the presence of the conserved 30-amino acid sequence in the first annexin repeat, which has similarity to heme binding domain of plant peroxidases (Gorecka et al., 2005; Jami et al., 2008; Laohavisit et al., 2009) [18, 24 32] . This peroxidase like motif contains critical conserved His + residue needed for haeme-binding domains that overlaps with the Ca +2 -binding site in the first repeat, raising the possibility that Ca +2 could regulate this peroxidase activity observed in annexins. The production of H 2 O 2 is induced by several different biotic and abiotic stresses and helps to maintain plant responses to these stresses. So, the annexinperoxidase connection raises the possibility that annexins could play a role in preventing the accumulation of damaging levels of this agent. Jami et al. (2008) [25] found that excised mature leaves from AnnBj1 overexpressing tobacco transgenic plants showed 1.8-2.6-fold more total peroxidase activity compared to wild type plants under oxidative stress. Studies on the over expression of AnnBj1 in cotton showed an increase in total peroxidase activity ranging from 2.1-2.8-fold in transgenic plants and corresponding reduction of H 2 O 2 contents when compared with the control plants under all stress (salinity, dehydration and oxidative stress) treatments (Divya et al., 2010) [13] . This is corroborated by the significantly enhanced fluorescence detected by H 2 DCFDA in the stomatal guard cells of wild type plants than the transgenic plants which showed less fluorescence due to ROS detoxification. This activity could be attributed to the constitutively expressed AnnBj1 gene. Similarly, Konopka-Postupolska et al., (2009) [29] observed significantly reduced levels of ABA induced ROS identified by the fluorescent dye, H 2 DCFDA, in AnnAt1 over expressed Arabidopsis lines compared to WT plants. Transgenic cotton plants over expressing annexin gene, CkANN, displayed significantly higher peroxidase activities compared to control plants when inoculated with Fusarium oxysporum (Zhang et al., 2011) [55] . Over expression of various annexin genes in tobacco and cotton transgenic plants displayed significant retention of total chlorophyll content and lower levels of TBARS with reduced lipid peroxidation and membrane damage in comparison to WT plants which displayed damaged membrane by more lipid peroxidation resulting in susceptibility to stress treatments (Jami et al., 2008; Divya et al., 2010; Zhang et al., 2011) [24, 55,13]. These results are implying that annexins have a protective role in the stress induced membrane damage. Accumulation of ROS results in formation of MDA levels in plants due to membrane lipid peroxidation. Under salt and drought stress treatments transgenic cotton plants over expressing GhAnn1 shown increased SOD activity with improved ROS detoxification thereby low MDA accumulation, less membrane damage, and more stable cell membrane (Zhang et al., 2015) [54] .

Annexins in osmotic stress tolerance

High levels of salinity and drought in plant cells leads to cellular ions imbalance and finally osmotic stress. Plants respond to osmotic stresses by osmotic adjustments through accumulation of osmoprotectants. Many studies have shown that free proline and soluble sugars are the most widely distributed multifunctional osmoprotectants to counter the stress induced by salt and drought stresses. To elucidate the role of annexins in osmotic stress tolerance, the levels of free proline and soluble sugars were estimated in wild type and transgenic plants over expressing various annexin genes under drought and salinity stress. Divya et al. (2010) [13] observed enhanced levels of free proline and soluble sugars (fructose, glucose and sucrose) content in AnnBj1 over expressing cotton plants which was significantly very high compared to the WT plants under 400 mM NaCl stress. It was demonstrated that the modulation in cytosolic Ca 2+ during salt stress can regulate the gene expression of P5CS encoding enzyme responsible for conversion of glutamate to proline in the proline biosynthesis pathway (Parre et al., 2007; Divya et al., 2010) [38,13] . Semi-quantitative RT-PCR analysis recorded conspicuously higher expression levels of P5CS, which was consistent with the enhanced proline content in AnnBj1 over expressing cotton transgenic plants under salt stress (Divya et al., 2010) [13] . Previous studies have shown that over expression of proline biosynthesis genes in transgenic plants conferred salt stress tolerance (Kishor et al., 1995; Reddy et al., 2015) [28,41] . Similarly, enhanced levels of free proline and soluble sugars were observed in GhAnn1 and CKANN over expressing transgenic cotton plants compared to WT plants under salt and drought stress conditions respectively (Zhang et al., 2011; Zhang et al., 2015) [55,54] . Accumulation of soluble carbohydrates as osmoprotectants during osmotic and salinity stresses is one of the alternate tolerance mechanisms developed by the plants and stress induced soluble carbohydrates conferring stress tolerance has been demonstrated (Kerepesi and Galiba, 2000) [27] . Sucrose accumulation can increase cytosolic calcium levels by producing Ca 2+ influx. Enhanced cellulose deposition in fibers translocated from the enhanced sucrose pools in the leaves during elongation and secondary wall synthesis determines the fiber quality. Transgenic cotton plants over expressing Indian mustard annexin gene had significantly high proportion of better quality well developed mature fibers with higher cellulose content compared to WT plants under salt stress. This result implying the role of annexin in the cellulose biosynthesis pathway (Divya et al., 2010) [13] . Taken all together, these experimental evidences indicate that annexins play a protective role in enhanced drought and salt stress tolerance.

Abbreviations

References

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