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Fehér, A. The Molecular Identity of Plant Callus Tissues. Encyclopedia. Available online: https://encyclopedia.pub/entry/52654 (accessed on 17 July 2025).
Fehér A. The Molecular Identity of Plant Callus Tissues. Encyclopedia. Available at: https://encyclopedia.pub/entry/52654. Accessed July 17, 2025.
Fehér, Attila. "The Molecular Identity of Plant Callus Tissues" Encyclopedia, https://encyclopedia.pub/entry/52654 (accessed July 17, 2025).
Fehér, A. (2023, December 13). The Molecular Identity of Plant Callus Tissues. In Encyclopedia. https://encyclopedia.pub/entry/52654
Fehér, Attila. "The Molecular Identity of Plant Callus Tissues." Encyclopedia. Web. 13 December, 2023.
The Molecular Identity of Plant Callus Tissues
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This entry is adapted from the peer-reviewed paper 10.3390/ijms241713122

In response to different degrees of mechanical injury, certain plant cells re-enter the division cycle to provide cells for tissue replenishment, tissue rejoining, de novo organ formation, and/or wound healing. The intermediate tissue formed by the dividing cells is called a callus. Callus formation can also be induced artificially in vitro by wounding and/or hormone (auxin and cytokinin) treatments. The callus tissue can be maintained in culture, providing starting material for de novo organ or embryo regeneration and thus serving as the basis for many plant biotechnology applications. Due to the biotechnological importance of callus cultures and the scientific interest in the developmental flexibility of somatic plant cells, the initial molecular steps of callus formation have been studied in detail. It was revealed that callus initiation can follow various ways, depending on the organ from which it develops and the inducer, but they converge on a seemingly identical tissue. However, the common molecular signature that the various pathways converge on and define calli, regardless of their variable origin, as the same tissue has not yet been revealed.

callus gene expression organ primordium meristem transcription factor auxin cytokinin plant regeneration

1. Introduction

Higher plants (referred to only as “plants” hereinafter), as sessile organisms, are repeatedly exposed to abiotic factors (e.g., wind, fire) and biotic agents (e.g., herbivores) that damage their structural and functional integrity. Plants can cure smaller damages via tissue repair, during which they reconnect severed organs, such as stems and petioles [1][2]. However, the damage can result in the loss of large parts of the plant involving one or several organs. Therefore, plants have evolved so that they do not have irreplaceable individual organs, such as the brain or the heart of animals, that would cause them to die if damaged. Instead, plants have a modular design that ensures their survival even if several of their numerous identical organizational units, called “phytomers” [3], are lost. Phytomers are constantly produced by the apical meristems underlying plant growth and replacing old, non-functional, or lost organs with new ones. The phytomers are not only structural but also fully functional developmental units. They themselves have post-embryonically formed meristems, which, besides allowing branching, can replace the apical meristem [4][5]. However, the regeneration ability of plants goes far beyond activating preexisting dormant meristems. New meristems can de novo form from differentiated tissues of adult plants. For example, when the tip of a plant shoot or root is partially or entirely removed, the cells at the wound site undergo a process of reprogramming, restoring the apex that contains a new apical meristem [1][2][6][7][8][9][10]. Meristems can even develop at places where no meristem existed before, leading to adventitious root, shoot, or even embryo formation [11]. The regeneration ability of higher plants is so extreme that even an isolated single cell can be regenerated into a whole plant, although only under artificial in vitro conditions [12][13][14].
The extreme regeneration ability of plants is widely explored for biotechnological applications, including cloning and mass propagation of selected individuals, production of virus-free plants, grafting, and genetic modifications at the cell level (mutagenesis, cell hybridization, genetic transformation, genome editing, etc.) followed by the regeneration of genetically modified whole plants [15][16][17]. Due to the wide impact of this technology on plant breeding and biotechnology, in vitro regeneration systems have been elaborated for countless plant species. Nevertheless, despite the considerable recent progress in the understanding of the molecular background of plant regeneration [18][19][20], there are still significant gaps in our knowledge, preventing the genotype-independent general application of the technology [21].
Many in vitro plant regeneration systems include the intermediate formation of so-called callus tissue. Besides serving as an intermediary phase in plant regeneration, callus cells can be cultured as cell suspensions in various bioreactors to produce useful metabolites [22]. Although plant callus cultures are central in many plant biotechnology applications, the definition of a plant callus tissue is a question of debate. The reason behind it is that calli can form in various ways and exhibit various characteristics, depending on the plant species, genotype, source tissue, induction, and culture conditions, etc. [21][23]. The general view is that a plant callus is an unstructured non-specialized tissue formed by dividing parenchymatic cells. Furthermore, the callus is often, and wrongly, considered a “dedifferentiated” cell mass [21].
Plant callus forms naturally as a wound-healing tissue [24][25] or as a plant tumor in response to pathogens or genetic disorders [26]. In vitro, callus formation is achieved via the application of plant hormones, with or without wounding (for review [23][27]. The appropriate ratio of auxin and cytokinin is considered the most potent inducer of it [28][29]. A complex network of transcription factors (TFs) is implicated in callus initiation (for review [23]). Callus formation also occurs in plants due to the ectopic or missing expression of key genes involved in developmental regulation (for review [23]). Environmental cues, including light, temperature, and the presence of pathogens, also influence the formation of calli [1]. In agreement with the various explants and conditions used for callus initiation and culture, plant calli are not uniform, neither morphologically nor in their developmental potential. They can vary in color (white, yellow, green, brown), their compact or friable structure, their dependence on plant hormones for cell division, and their regeneration potential (non-regenerating, rooty, shooty, or embryogenic) [26]. Based on the diversity of callus tissues, it is not surprising that the initial steps of their formation can also be quite different. Below I overview the molecular control of wound and auxin-induced callus formation. Details about tumor formation in plants due to genetic and/or environmental perturbations of plant development can be found in the recent review of Dodueva et al. [26].

2. Molecular Signature of Callus Tissues

2.1. The Induction Phase

The steps of the signaling pathways leading to callus formation exhibit considerable differences depending on the organ, the inducer, and the plant species. The same holds true for the molecular landscapes of the formed initial callus tissues [21]. While the CIM-induced callus (CIM stands for the auxin- and cytokinin-containing callus induction medium) exhibits a gene expression pattern resembling that of the root meristem [30], it is not the case if the callus forms in response to wounding [23][31]. Even in the case of the same callus induction method, the upregulated genes significantly differ depending on the initial explant and even from experiment to experiment [32][33] with only 400 DEGs in common. The initial events of callus induction by CIM, not surprisingly, include the upregulation of auxin-related molecular pathways, which likely differentially affected downstream genes depending on the type and condition of the explant. This obviously resulted in highly divergent gene expression patterns. From these studies, there is no clue to answer the question of whether established callus tissues formed from different explants in response to various inducers share a common gene expression pattern that can define them as a specific tissue.

2.2. Young Calli

An attempt to compare gene expression in in vitro cultured plant cells to that of seedlings led to the recognition of the WIND1 TF as a “dedifferentiation” factor [34]. In a follow-up study, differentially expressed genes (DEGs) in wound-(35S:WIND1) and auxin-(2,4-D) induced two-week-old “young” calli were identified in reference to gene expression in uninduced seedlings [31]. Several hundred genes could be determined, the upregulation of which in callus cells was independent of the way of induction. Among these genes, 21 codes for AP2/ERF domain TFs including the regeneration-related WIND1, ESR1, Rap2.6L, ERF114, PLT3, 5 and 7. Lee and their colleagues reported differential gene expression in two-week-old CIM-induced calli developing on leaf explants [35]. The overlap among the DEGs in these calli (5708 genes) and the strong callus upregulated gene list of Iwase and their colleagues (658 genes; upregulated both in 35S:WIND1- and 2,4-D-induced calli) is rather limited, highlighting only 232 genes. Interestingly, this common list is enriched in genes expressed in response to stress, especially hypoxia. Nevertheless, the auxin-responsive ARF5/MP was present in all the above datasets, such as the regeneration-related ones, Rap2.6L, ERF114, PLT3, and PLT5, while WIND1 was not among the DEGs in the leaf callus study. Interestingly, if we compare the 400 DEGs obtained four days after 2,4-D-induction (at the time of first cell divisions) with the 232 DEGs of young calli (two weeks after induction), there is an overlap of only 35 genes, indicating a continuing reorganization of the gene expression pattern during the first weeks of callus establishment.

2.3. Established Callus Cultures

Calli can be maintained as cell suspension cultures for a long time in the presence of auxin and cytokinin. It is, therefore, a valid question how the initial gene expression pattern of callus cells is preserved during long-term culture. Iwase and colleagues [31] compared the DEGs in 35S:WIND1 and 2,4-D-induced calli to those of the T87 cell suspension culture (all DEGs were defined in comparison to seedlings). Out of the 232 upregulated DEGs of 35S:WIND1 and 2,4-D-induced calli, 144 were also upregulated (at least two-fold) in the T87 cell culture. This gene set is enriched in stress-related genes, especially those responding to hypoxia, as well as in hormone-responsive ones. Among the upregulated DEGs of callus induction, in young calli and in established cell cultures, there are 21 that are common. Although stress-related genes are prevalent in all callus-related gene expression datasets, and one would expect cell division-related genes to be upregulated in all callus tissues that have dividing cells, the 21 common genes that are expressed in all types of callus cell are neither strictly stress- nor cell division-associated. Importantly, however, the list of these 21 genes contains six TF genes with functions in meristematic, organ primordial, provascular tissues.

3. What Can Callus-Expressed Genes Teach Us?

One of the TF genes expressed in all types of calli investigated is the auxin response factor ARF5/MP gene, a key regulator of cell specification during both embryogenic and post-embryogenic development. During Arabidopsis embryogenesis, ARF5/MP cell-autonomously controls vascular and ground tissue initiation, while root meristem specification depends on non-cell-autonomous ARF5/MP action [36]. ARF5/MP is also expressed during LR initiation and meristem formation [37]. In the emerging lateral root primordia (LRPs), ARF5/MP expression was prominent in the central cell files and excluded from the flanks [38][39]. ARF5/MP is also present in the shoot apical meristem (SAM), not only in the dividing cells of the meristem but also in the differentiating cells of the lateral organ primordia [37][40][41]. The ARF5/MP gene was activated in the pericycle cells all over the root explants placed on CIM [42]. ARF5/MP remained abundant in the dividing and then rapidly proliferating pericycle-derived cells forming the callus. A constitutively active variant of ARF5/MP promotes shoot organogenesis [42]. Altogether, ARF5/MP is an important regulator of ground, vascular, and stem cell identities, meristem maintenance and function, and the initiation of lateral organ primordia and a good candidate to maintain the auxin-dependent cell division activity as well as the organogenic potential of calli.

The TF PLETHORA3 (PLT3) can have similar importance and role in the callus cell fate. PLT3 belongs to the AINTEGUMENTA-LIKE (AIL) TF family and is also designated as AIL6. AIL6/PLT3 expression is undetectable during early embryogenesis, but at later stages, it is confined to the QC and the surrounding cells, including the ground tissue and provascular cells [43][44]. During LR formation, PLT3, PLT5, and PLT7 redundantly control the first events, including the first formative cell divisions and the establishment of growth polarity. Their action is a prerequisite for the subsequent specification of the LR meristem, controlled by PLT1, PLT2, and PLT4 [45]. AIL6/PLT3, together with AINTEGUMENTA (AINT) and PLT7, play a significant role in the maintenance and functioning of the shoot apical meristem as well [46]. AIL6/PLT3 is expressed in the center as well as in the periphery of the SAM, indicating its role both in meristem maintenance and lateral organ formation in the shoot, such as in the root [46][47]. It is obvious that ARF5/MP and AIL6/PLT3 control very similar processes during plant development. Nevertheless, there is only limited data available about their interlinked action [48][49].

Considering the overlapping key roles of ARF5/MP and AIL6/PLT3 in plant growth, organ formation, and tissue patterning, it was obvious to ask the question of whether the other nineteen callus genes also have related functions, despite their seemingly non-related functional annotations. Most of these 19 genes, inaddition to ARF5/MP and AIL6/PLT3 could be somehow linked to meristem, lateral organ, and/or vascular development, respectively, although at different levels. The two other transcription factors, WRKY23, and SPT, both having roles in spatial and temporal regulation of meristem and organ primordium initiation (including the formation of the vasculature) and maintenance, deserve special attention. The strong expression of callus-related genes especially of ATDI21, but also of ATF6, COBL1, and PLL1 in various meristematic cell types including callus tissues should prompt us to investigate their cellular functions in more detail.

The gene expression domain of these factors during the early phases of embryogenesis and organ formation is the internal domains of the embryo and the organ primordia comprising the dividing ground tissue with pre-vascular cells. Shoot and root meristem initials, as well as pro-cambial cells, arise within this domain due to the establishment of spatially controlled hormonal and molecular feedback mechanisms. During callus formation, however, these feedback mechanisms are not formed due to disturbed developmental control. Therefore, callus cells are blocked in a kind of pre-meristematic state and keep the associated gene expression signature, including the expression of the ARF5/MP, AIL6/PLT3, SPT, WRKY23 and the further 17 callus-signature genes. The function of some of these genes is maintaining the cell division activity until appropriate hormonal signals are provided exogenously or endogenously. This pre-meristematic tissue state might explain the organogenetic potential of most callus tissues. Under appropriate conditions, endogenous hormone gradients can reestablish on the surface of the cell colonies to organize shoot- or root meristem or both (i.e., somatic embryo), a phenomenon widely used in plant biotechnology [19]. Obviously, as callus growth, metabolic and hormonal gradients may establish within the tissue leading to various degrees of cellular heterogeneity, especially between the outer and inner domains, that can lead to the loss of cell division and/or organogenic potentials.

4. What Is a Plant Callus?

Plants can regenerate lost tissues and organs due to competent cells responding to injuries with cell divisions followed by cell differentiation. This differentiation step is under the control of the short- and long-term morphogenic signals of the damaged region, ensuring that the proper cell, tissue, or organ forms in the right place. However, if these signals are not present or seriously disturbed, cells may continue to divide forming an ill-organized organ primordium. This primordium cannot establish the inner meristematic and the outer non-dividing domains, which mutually regulate each other, but gets blocked in a kind of pre-meristematic ground-tissue state. This state is characterized, among other things, by the expression of the ARF5/MP, AIL6/PLT3, SPT, and WRKY23 transcription factor genes, the DI21 gene with an unknown function, and several other genes that have been implicated in provascular/procambial cells. In the presence of auxin and cytokinin (either exogenous or endogenous) the cells further divide in an unorganized way to form what is known as callus tissue. Thus, considering its molecular nature and developmental potantial, callus resemble of the central ground tissue of early embryos/organ primordia with the potential to form meristematic (including procambial) or parenchymatic cells depending on internal/external signals.

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