Functional Mechanisms and the Application of Developmental Regulators for Improving Genetic Transformation in Plants

Abstract

Enhancing the genetic transformation efficiency of major crops remains a significant challenge, primarily due to their suboptimal regeneration efficiency. Developmental regulators, known as key regulatory genes, involved in plant meristem and somatic embryo formation, play a crucial role in improving plant meristem induction and regeneration. This review provides a detailed summary of the molecular mechanisms and regulatory networks of many developmental regulators, in the context of enhancing the genetic transformation efficiency in major crops. We also propose strategies for exploring and utilizing additional developmental regulators. Further investigation into the mechanisms of these regulators will deepen our understanding of the regenerative capacity and genetic transformation processes of plants, offering valuable support for future crop improvement efforts. The discovery of novel developmental regulators is expected to further advance crop transformation and the effective manipulation of various developmental regulators could provide a promising approach in order to enhance genetic transformation efficiency.

1. Introduction

With the growing global population and the increasing pressure from climate change on agricultural production, traditional plant breeding methods are becoming inadequate to meet the demands of food security and sustainable development [1,2]. In these circumstances, plant genetic transformation technology has become an indispensable tool in modern agriculture, offering a wide range of potential applications. Efficient genetic transformation techniques are fundamental to gene-editing technologies (such as CRISPR/Cas9), which enable precise genome modifications, and to biotechnological breeding methods (such as transgenic breeding) [3,4], thereby significantly accelerating the plant breeding process. Moreover, gene function analysis, including both forward and reverse genetics, also relies on genetic transformation techniques to clarify the roles of specific genes in plant growth and development [5,6,7,8,9,10]. Stable and efficient transformation systems are crucial for both gene knockout and overexpression studies [11,12].

Beyond accelerating plant breeding and elucidating gene function, genetic transformation technology also plays a critical role in ensuring the safety and regulatory compliance of gene-edited and transgenic crops [3,13]. For instance, precise transformation techniques are essential to minimize off-target effects and unintended genetic modifications [14], thereby enhancing the safety and acceptance of genetically modified organisms (GMOs) and gene-edited plants [3]. Genetic transformation techniques further support the development of biosafety management strategies, such as better control of gene flow, the monitoring of environmental impacts, and the assessment of potential risks to human health. Additionally, transformation methods are indispensable for optimizing trait stacking, which involves the simultaneous introduction of multiple desirable genes into plants to enhance complex traits, such as drought tolerance, pest resistance, and nutritional quality [3]. This multifaceted application underscores the importance of genetic transformation technology not only in crop improvement, but also in addressing the challenges of sustainable agriculture in a changing global environment [15].

However, current plant genetic transformation technologies face significant challenges, such as strong genotype dependency, low regeneration efficiency, and the complexity of the transformation process, particularly in crops that are difficult to transform. To address these challenges, researchers have successfully developed various developmental regulators (DRs) to promote plant regeneration and enhance transformation efficiency. These DRs include SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) [16,17], LEAFY COTYLEDON (LEC) [18,19,20], WOUND-INDUCED DEDIFFERENTIATION 1 (WIND1) [20,21,22], BABY BOOM (BBM) [23,24,25,26], WUSCHEL (WUS) [27,28,29,30,31,32], the growth-regulating factor–growth regulator interacting factor (GRF–GIF) complex [33,34,35,36], the WUSCHEL-RELATED HOMEOBOX (WOX) [37,38,39,40,41,42], rZmGOLDEN2 [43], DNA binding with One Finger (DOF) [44], and REGENERATION FACTOR 1 (REF1) [45]. By modulating the expression of these DRs, significant improvements in the formation efficiency of meristems and somatic embryos have been achieved, thereby increasing the success rate of genetic transformation. However, the molecular mechanisms according to which these DRs function across different species and genotypes are not yet fully understood, which limits their broader application in agricultural production.

In this review, we focus on summarizing and analyzing the latest progress in the application of DRs in terms of plant genetic transformation, elucidating their roles in enhancing genetic transformation efficiency and exploring their potential application values across different plants. Additionally, we discuss strategies to optimize the combination and application of these DRs to overcome existing bottlenecks in genetic transformation technologies and provide new directions for future research.

2. Developmental Regulators for Plant Genetic Transformation: Mechanisms, Advances, and Applications

2.1. WUS and BBM Promote Genetic Transformation in Plants

WUSCHEL (WUS) and BABY BOOM (BBM) are key regulatory factors of cellular totipotency and they can promote cell dedifferentiation and somatic embryogenesis, which have been corroborated across a variety of plant species, including Arabidopsis (AtWUS and AtBBM) [29,30,46], maize (Zea mays L.) (ZmWUS2 and ZmBBM) [31], and rice (Oryza sativa) (OsBBM) [31]. OsWUS is essential for rice tiller development, as it regulates apical dominance and hormonal responses that influence tiller bud outgrowth [47]. WUS promotes the integration of exogenous DNA into receptor genomes by maintaining plant receptor cells in an undifferentiated state [48], while BBM triggers somatic embryogenesis and facilitates cell proliferation and division [49]. The expression of both genes can significantly enhance the genetic transformation efficiency of difficult-to-transform plant varieties and promote the formation of callus tissue and the regeneration of transformed plants [31].

The synthesis and signaling of plant hormones, particularly auxins and cytokinins, are crucial for maintaining cell fate and organ formation [50]. The functional mechanisms of WUS and BBM are intricately linked to these hormone signaling networks. Both WUS and BBM transcriptionally regulate LEAFY COTYLEDON1 (LEC1), LEC2, and AGAMOUS-LIKE15 (AGL15) to enhance embryonic competence during somatic embryogenesis [49] (Figure 1). LEC further modulates downstream hormone signaling pathways. WUS and Arabidopsis Response Regulators (ARRs) positively and negatively regulate cytokinin signaling, respectively [51,52] (Figure 1). The synthesis of auxins, regulated by Tryptophan Aminotransferase of Arabidopsis 1 (AtTAA1), YUCCA3 (AtYUC3), and AtYUC8, along with auxin polar transport mediated by pin-formed 1 (NtPIN1) and NtPIN2, and signal transduction mainly by indole-3-acetic acid (AtIAA) and Auxin Response Factor (AtARF) family members, collectively influence the differentiation process of transformed cells [49,53] (Figure 1). Concurrently, the gibberellin metabolic pathway, regulated by GA20-oxidase genes (AtGA20ox6 and AtGA3ox2), and cell proliferation-related factors, such as the Actin depolymerizing factor (AtADF9) [54,55], play key roles in enhancing genetic transformation efficiency. LEC1/2 (e.g., AtLEC1/2) and MADS-box transcription factor AGAMOUS-LIKE 15 (e.g., AtAGL15) participate in regulating embryonic development and cell proliferation [49], thus constructing a complex regulatory network. The integrated action of WUS and BBM promotes cell proliferation and shoot formation more efficiently than either gene alone and increases the likelihood of successful transformation events, which can result in the growth of viable transgenic plants. Their synergistic effects greatly increase the genetic transformation efficiency of various plant species, such as maize, rice, and Arabidopsis, as well as sorghum (Sorghum bicolor), coffee plants, and hemp (Cannabis sativa) (Figure 1).

The overexpression of WUS and BBM has been identified as significantly improving the transformation efficiency of various plants. Lowe et al. were the first to overexpress ZmBBM and ZmWUS2 in immature maize embryos, and the transformation efficiencies of several previously deemed difficult-to-transform maize inbred lines were significantly improved (Table 1) [31]. Additionally, they successfully transformed mature seed embryos and leaf segments from different inbred line seedlings with overexpressed ZmBBM and ZmWUS2 and then obtained normal T₀ plants. This method significantly enhances the genetic transformation efficiency and reduces the genotype dependency in maize [31].

However, the ectopic expression of both ZmBBM and ZmWUS2 adversely affected the growth of regenerated plants [31]. To mitigate these negative impacts, especially on the growth and fertility of transgenic maize plants, Lowe et al. employed the ZmPLTP (phospholipid transfer protein gene) promoter and the auxin-inducible ZmAxig1 promoter to drive ZmBBM and ZmWUS2, respectively (Table 1) [56]. This strategy enhances the tissue- and temporal-specificity of the expression of both genes and allows maize to be efficiently and rapidly genetically transformed, overcoming specific genotype dependency and bypassing the callus culture stage. Notably, ZmPLTP and Axig1 promoters are active only when using immature embryos (IEs) as explants. This approach rapidly produces a large number of somatic embryos (SEs) that are directly transformed and grown into plants without the callus stage, and the resulting transgenic plants display normal growth and reproductive capabilities [56].

The prolonged expression of certain DRs leads to abnormal seedlings, which thus need to be removed after the transformation process. Wang et al. explored a new strategy by utilizing the inducible Cyclization Recombination Enzyme (CRE) to remove DRs [57]. During this strategy, the promoters of genes encoding inducible heat-shock proteins, such as Hsp17.7 and Hsp26, were used to drive CRE expression during the early embryo development stages to remove unnecessary transgenic elements in regeneration plants. This method, combined with improved tissue culture conditions, can achieve higher T₀ transformation rates and reduce the occurrence of non-transgenic transformants, thereby improving the transformation efficiency of specific maize inbred lines (Table 1). Additionally, it ensures that the transformants do not contain DRs and/or selection markers, thus providing a more efficient tool for precise genetic improvement.

In plant genetic engineering, the ternary vector system, by combining disarmed Ti plasmids, T-DNA binary vectors, and additional helper plasmids [58], enhances the virulence functions, thereby improving the efficiency of the T-DNA transfer into the plant genome. The cooperative action initiated by additional virulence genes in the system further boosts the transformation efficiency [58]. The ternary vector system is designed for broad applicability across different Agrobacterium strains, while the transformation efficiency varies when using different strains. Thus, optimization is required for specific plant species and experimental conditions. The ternary vector system, combining CRE-assisted transgene elimination, is commonly applied to further enhance maize transformation efficiency. Specifically, a ternary vector system was designed to integrate the CRISPR/Cas9 genome-editing module with a CRE excision system, driven by a drought-inducible promoter (Rab17) [59]. The novel ternary vector system primarily consists of a new dual-component pGreen-like vector, pGreen3, along with a virulence auxiliary vector, based on pVS1 and a pGreen3 replication auxiliary vector. In conjunction with the DR module, this ternary vector system significantly enhances the Agrobacterium-mediated transformation efficiency in maize (Table 1) [59].

Table 1

Developmental regulators improving genetic transformation in plants.

Developmental Regulators	Encoding Proteins	Genes	Species	Explants	Transformation Effects	Refs.
BABY BOOM (BBM); WUSCHEL (WUS)	BBM, transcription factors of the AP2/ERF family; WUS, a homeodomain transcriptionfactor	ZmBBM; ZmWUS2	Zea mays	Immature embryo;mature seed embryo sections;seedling-derived leaf segments	Significantly increases transformation efficiency and reduces genotype dependence for inbred PHH5G, PHP38, PHN46, PH581, and PH0AZ	[31]
				Immature embryo	Healthy and fertile plants are regenerated	[56]
					Transgenic plants are free of morphogenic and marker genes	[57]
					Transformation frequencies increase by 20 times in recalcitrant maize inbred line ND88	[59]
				Seedling-derived leaf tissue	Substantially improves leaf transformation for inbred PH1V69 and B104	[32]
			Sorghum	Seedling-derived leaf tissue	The average frequency of T0 sorghum (Tx430 variety) plants in the experimental group ranges from 35% to 37%	[32]
			Eragrostis tef	Seedling-derived leaf tissue	T0 seedlings with healthy shoots and roots were regenerated	[32]
			Panicum virgatum
			Cenchrus americanus
			Setaria italica
			Secale cereale
			Hordeum vulgare
		ZmWUS2	Zea mays	Immature embryo	Removal of the morphogenic genes and high transformation frequencies for inbred PHW52, PH2KD1, PH28SV, PH4BAH, PH2Y8G, and PH4B9Z	[60]
		OsBBM; ZmWUS2	Oryza sativa	Calli	Transformation frequencies increase by 13 times for indica variety IRV95	[31]
		ZmBBM; ZmWUS2			Transformation frequencies increase by eight times for indica variety IRV95
		AtWUS	Medicago Sativa	Leaflets and hairy root segments	The number of embryos produced per WUS callus was 76% and 2.3-fold higher than that of the control	[61]
		HvBBM; HvWUS	Hordeum vulgare	Immature embryo	The transformation frequency significantly exceeded the empty vector control by 17.48%	[62]
		BnBBM	Capsicum annuum	Cotyledon segment	Compared to the control group with no transgenic plantlets, the transformation efficiencies for the experimental groups were 0.6% and 1.1%, respectively	[26]
		TcBBM	Theobroma cacao	Cotyledon	Somatic embryo production per explant was 29% higher compared to the control tissue	[63]
		AtWUS	Gossypium hirsutum	Hypocotyl segment	The differentiation rate of 35S/WUS transgenics was 47.14% higher than that of the control group	[30]
		AtWUS	Coffea canephora	Leaf segment	Expression of WUS in coffee plants induces callus formation and boosts somatic embryo production by 400%	[64]
		MdBBM1	Malus domestica	Leaf segment	The transformation efficiencies were 250% to 327% higher compared to the control group	[65]
		CsWUS4	Cannabis Sativa	Hypocotyls from immature grain	The shoot regeneration frequency increased by 170%	[66]
WUSCHEL-RELATED HOMEOBOX (WOX)	WUSCHEL-RELATED HOMEOBOX (WOX) family protein	TaWOX5	Triticum aestivum	Immature embryo	Much higher transformation frequencies (up to 1.9 times) in 29 wheat (Triticum aestivum) varieties	[42]
			Zea mays		Transformation frequencies of 19–38% in B73 and A188
		ZmWox2a	Zea mays		Production of phenotypically normal and fertile regenerants for inbred lines B73 and LH244	[67]
Growth-regulating factor–growth regulator interacting factor (GRF–GIF)	GRF protein with conserved QLQ and WRC domains and GRF-interacting factor	TaGRF4; TaGIF1	Triticum aestivum	Immature embryo	A maximum enhancement of up to 7.8-fold in regeneration efficiency is observed among cultivars, including Kronos, Desert King, Cadenza, Cadenza, and breeding line UC3184	[34]
			Oryza sativa	Mature embryos	The regeneration efficiency increased 2.1 times in the variety Kitaake
		CsGRF4; CsGIF1	Citrus	Epicotyl	The regeneration frequency increased by 370%
		ZmGRF5-LIKE1; ZmGRF5-LIKE2	Zea mays	Immature embryo	Transformation frequencies increase by three times for inbred line A188	[35]
		AtGRF5; GmGRF5-LIKE	Glycine max L.	Seedling	More shoot development per explant in cultivars Jake and CD215
		AtGRF5	Beta vulgaris ssp. vulgaris	Leaf from micropropagated shoots	A significant 6-fold increase in the transformation efficiency
		HaGRF5-LIKE	Helianthus annuus	Cotyledon	Promotes transgenic shoot production
		ClGRF4; ClGIF1	Citrullus lanatus	Cotyledon	The regeneration efficiency increased by 19.64% to 67.27%	[36]
DOF	DNA binding with One Finger	TaDOF5.6 TaDOF3.4	Triticum	Immature embryo	A maximum enhancement of up to 2.12 times in regeneration efficiency is observed in Fielder, JM22, and Kenong 199	[44]
GOLDEN2	Members of the GARP (Golden2, ARR-B, and Psr1) superfamily of transcription factors	rZmGOLDEN2	Zea mays	Immature embryo	Transformation frequency improvements of 1.75 times for inbred line B104	[43]
			Oryza sativa	Calli	Transformation frequency improvements of 1.31–3.44 times for HuaZhan, HuaGuang, DongJing,and ZhongJia 8
REF1(REGENERATION FACTOR 1)	The precursor of SlPep, the sole tomato ortholog of the plant elicitor peptide (Pep) family of immunomodulatory peptides	SISPR9	Tomato(Solanum lycopersicum)	The stem base of 18-day-old tomato seedlings	Increased the transformation efficiency of the wild tomatoes S. peruvianum and S. habrochaites by 6 to 12 times	[45]
		GmREF1	Glycine max L.	Cotyledonary nodes	Increased the transformation efficiency of Dongnong-50 by 2–5 times
		TaREF1	Triticum	Immature embryo	Increased the transformation efficiency of JM22 by four times
		ZmREF1	Zea mays	Immature embryo	Increased the transformation efficiency of B104 by four times
LAX1 (LAX PANICLE 1)	Non-canonical basic helix–loop–helix transcription factor	TaLAX1	Triticum	Immature embryo	Significantly increased the transformation efficiency of the wheat varieties Fielder and Chinese Spring	[68]

In addition to their application in major crops, WUS and BBM have also been utilized in horticultural and medicinal plants (Figure 1; Table 1). For instance, expressing AtWUS in coffee plants (Coffea canephora) can induce the formation of callus tissue and increase the amount of somatic embryos by 400% [64]. The ectopic expression of the MdBBM1 gene in apple plants (Malus domestica Borkh) leads to enhanced mRNA levels of cell division activators and reduces those of inhibitors associated with hormonal (auxin, cytokinin, and gibberellin) signaling pathways, which together significantly improve the genetic transformation efficiency in apple plants [65]. Additionally, a recent study has shown that overexpressing DR genes, such as CsGRF3–CsGIF1 and CsWUS4, in the hypocotyls of immature grains of hemp (Cannabis sativa) can significantly enhance shoot regeneration efficiency [66]. In summary, the functional mechanisms of WUS and BBM and their application in promoting genetic transformation efficiency in multiple plant species, especially in horticultural and medicinal plants, along with a deep understanding of their interaction with plant hormone regulatory networks, propel the development of advanced genetic transformation strategies required for plant genetic engineering.

2.2. Overexpression of SERK Enhances Somatic Embryogenesis

SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) belongs to the family of Leucine-Rich Repeat Receptor-Like Kinases (LRR-RLKs), characterized by their ability to recognize diverse extracellular ligands and transduce signals into the cell to trigger specific cellular responses [16,69]. In coffee plants, studies on the overexpression of CcSERK1 have elucidated its mechanism in regulating somatic embryogenesis by promoting auxin biosynthesis through activating key genes, such as CcAGL15, CcWUS, EMBRYOMAKER (CcEMK), CcBBM CcYUC1/4, and CcTAA1, and by promoting auxin transportation and signaling pathways through activating PIN1 and PIN4, which collectively lead to a significant increase in the number of somatic embryos [70] (Figure 2). Furthermore, SERKs are also considered as markers for identifying cells with embryogenic potential [71]. For instance, in rice, the suppression of OsSERK1 expression significantly reduces the bud regeneration rate, whereas its overexpression leads to the opposite result, highlighting its central role in somatic embryogenesis [71] (Figure 2).

2.3. WIND Regulates Cell Dedifferentiation in Wound Response

WOUND-INDUCED DEDIFFERENTIATION 1 (WIND1) belongs to the AP2/ERF transcription factor family, formerly known as RAP2.4 [21,72,73]. WIND1 can directly activate the expression of the ENHANCER OF SHOOT REGENERATION 1 (ESR1), encoding an AP2/ERF transcription factor in Arabidopsis, thereby promoting callus formation and bud regeneration [74] (Figure 2). Moreover, WIND1 also regulates cytokinin signaling, through activating ARR1 and ARR12, to promote callus formation at wound sites [75]. The ectopic expression of WIND1 not only induces callus formation and adventitious bud regeneration in Arabidopsis, but also induces callus formation in rapeseed (Brassica napus), tomato, and tobacco (Nicotiana tabacum), even on hormone-free media [22] (Figure 2). A recent study has demonstrated that the overexpression of ZmWIND1 can significantly increase the callus induction rates of maize inbred lines Xiang 249 and Zheng 58 to 60.22% and 47.85%, respectively. Additionally, the transformation efficiency was elevated to 37.5% in Xiang 249 and 16.56% in Zheng 58 [15]. Notably, the dual induction of WIND1 and LEC2 effectively promotes the formation of embryogenic calluses in rapeseed, while the induction of WIND1 or LEC2 alone is unable to successfully form a callus [76], offering a new strategy to enhance plant genetic transformation efficiency by combining WIND1 with other DRs.

Figure 2

Schematic representation of SERK, WIND1, WOX5, DOF, LBD, rZmGOLDEN2, and GRF–GIF and REF peptides and their roles in enhancing plant genetic transformation. Genes are color-coded by species: green for Arabidopsis, yellow for maize, blue for rice, dark gray for cotton, light gray for wheat, light orange for soybean (Glycine max), orange for Citrus, light purple for tomato, and light blue for poplar (Populus). The light blue font and boxes indicate hormone-related signaling pathways and associated biological processes, as well as their related genes. The genes shown above each plant species represent those employed to improve the genetic transformation efficiency in that particular species. The co-cultivation medium is primarily used for the Agrobacterium infection process and is not involved in the callus induction in explants. The processes illustrated reflect maize transformation, as an example.

[Figure omitted. See PDF]

2.4. WOX Involved in Promoting Somatic Embryogenesis

WOX5 is a primary regulatory factor involved in regulating the meristematic activity at root tips and stimulates cell differentiation by recruiting PLETHORA (PLT) factors [77]. Studies in Arabidopsis have shown that PLT3, PLT5, and PLT7 genes can coordinate to regulate de novo shoot regeneration through activating PLT1 and PLT2 genes to promote pluripotency establishment and through regulating CUP-SHAPED COTYLEDON2 (AtCUC2) to complete bud formation [78] (Figure 2). Additionally, studies have shown that PLT5 can promote in planta transformation in snapdragon (Antirrhinum majus) and tomato (Solanum lycopersicum), while significantly enhancing shoot regeneration and transformation efficiency in Chinese cabbage (Brassica rapa). PLT5 also facilitates the formation of transgenic calli and somatic embryos in sweet pepper (Capsicum annuum), through in vitro tissue culture [79].

In addition, WOX5 enhances callus tissue cell regenerative capacity through its transcriptional activator WRKY DNA-BINDING PROTEIN 23 (WRKY23) and repressor basic helix–loop–helix 041 (bHLH041) in Arabidopsis [80], demonstrating its significance in plant regeneration. In tobacco, combinations of WOX family members, WOX2, WOX8, and WOX9, promote plant regeneration [81]. Notably, in wheat, the overexpression of TaWOX5 significantly increases the genetic transformation efficiency [42] (Figure 2, Table 1), thus overcoming the challenge of wheat genotype-dependent transformation. This method is applicable to many commercial and hard-to-transform wheat varieties, in addition to Fielder and CB037. Further, the application of TaWOX5 in monocots, such as triticale (Triticum x Secale), rye (Secale cereale), barley (Hordeum vulgare), and maize, significantly improved their genetic transformation efficiency, for instance, as observed in maize inbred lines B73 and A188, whose transformation frequencies were significantly enhanced from 19% to 38% [42].

2.5. DOF TFs Boost Regeneration Efficiency

DOF (DNA binding with One Finger) proteins represent a plant-specific transcription factor family, initially identified in maize [82] and also in other eukaryotes [83]. TaDOF5.6 and TaDOF3.4 can enhance the genetic transformation efficiency in wheat [44]. The efficiency of callus induction by tissues transformed with TaDOF5.6 and TaDOF3.4 is increased from 26% to 50% and 55%, respectively (Table 1). Furthermore, TaDOF5.6 and TaDOF3.4 also enhance the callus induction rate and genetic transformation efficiency for the wheat varieties KN199 and JM22, which were originally difficult to regenerate [44]. In tissues transformed with TaDOF3.4 or TaDOF5.6, the expression levels of the root and shoot meristematic tissue-related genes LATERAL ORGAN BOUNDARIES DOMAIN 4 (TaLBD4) and SCARECROW-LIKE 27 (TaSCL27) are significantly elevated, and TaDOF3.4 directly activates the expression of TaLBD4 and TaSCL27 [44] (Figure 2). Hence, TaDOF5.6 and TaDOF3.4 are important DRs in promoting genetic transformation efficiency in wheat. However, there are no reports on DOF applications for genetic transformation in maize nor other crops.

2.6. LBD Transcription Factors Are Key Regulators of Auxin-Induced Callus Formation

The LBD/ASL (ASYMMETRIC LEAVES2-LIKE) gene family, with a highly conserved AS2/LOB (ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES) domain at its N-terminus, activates lateral root development to promote the formation of callus tissue [84,85,86]. Auxin response factors ARF7 and ARF19 regulate four downstream LBD genes, namely LBD16-18 and LBD29, which influence lateral root development and induce callus tissue formation [84]. Among them, LBD16 can directly activate FAD-binding berberine (FAD-BD), thereby promoting the formation of callus tissue [87]. In Arabidopsis, LBD18 activates EXPANSIN14 (EXP14) by directly binding to its specific promoter elements. EXP14 encodes a cell wall-loosening factor and promotes the occurrence of lateral roots [88] (Figure 2). This indicates that LBDs are involved in promoting cell proliferation during the formation of callus tissue. In cotton, the high level of expression of GhLBD18 is positively correlated with larger callus tissues and significantly accelerates the proliferation rate of callus tissue [89]. This process is effectively driven by the β-estradiol-inducible promoter pER8, thus offering a new strategy to replace traditional selective marker systems and provide new possibilities for enhancing cotton transformation efficiency and the genetic improvement capacity (Figure 2).

2.7. Overexpression of GOLDEN2 Promotes the Differentiation of Callus Tissue

GOLDEN2 (G2) is a member of the GARP transcription factor family, which includes ARR-B and Psr1 [90,91]. G2 contains the TEA domain and controls the development of chloroplasts and other biological processes [92]. Recently, the expression of rZmG2 in rice, which is codon optimized based on the maize G2 gene sequence, significantly improved the genetic transformation efficiency in rice [43]. Mature seeds of three rice varieties and the IE of a maize variety were used in this study to assess the role of the rZmG2 gene on the genetic transformation efficiency. As a result, transgenic maize and rice callus tissues exhibited early chloroplast formation and increased chlorophyll content during the differentiation stage, with a significant increase in the regeneration efficiency from 26% to 178.46% compared to wild-type callus tissue (Table 1). Further studies have revealed that chloroplast development-related genes, such as chlorophyll a/b binding protein 24 (OsCP24) and light harvesting chlorophyll a/b binding (OsLhcb2 and OsLhca4), are significantly upregulated in rice callus tissues carrying the rZmG2 gene. Additionally, the expression of plant hormone-related genes (e.g., small auxin-up RNA8 OsSAUR8) and late embryogenesis abundant (LEA) protein-encoding genes (OsLEA3, 14-16, and 22) are also affected [43] (Figure 2). Notably, the high level of expression of OsSAUR8 in transgenic callus tissues can promote differentiation by lowering the auxin concentration, as the differentiation of callus tissues requires a low ratio of auxin to cytokinin. During the genetic transformation of rice, the desiccation of callus tissues increases their regeneration potential. Thus, the low expression of LEAs in rZmG2 transgenic callus tissues is advantageous for reducing water retention, which can promote callus tissue desiccation and accelerate regeneration [43].

2.8. GRF–GIF Chimeras Enhance Plant Regeneration Efficiency

GRFs encode proteins containing QLQ (glutamine–leucine–glutamine) and WRC (tryptophan–arginine–cysteine) domains, which represent a class of plant-specific transcription factors [33]. The QLQ domain facilitates interactions between proteins and the WRC domain is involved in DNA binding [93]. GRFs interact with growth-regulating factor interacting factors (GIFs) to form a plant-specific transcription activation complex [33]. The GRF–GIF complex promotes organogenesis by activating a series of genes, such as HECATE1 (AtHEC1), HOMEOBOX PROTEIN 33 (AtHB33), CYTOKININ RESPONSE FACTOR 2 (AtCRF2), and CONSTANS-like 5 (AtCOL5) [94] (Figure 2). Additionally, AtGIF can repress the expression of the PLT1 gene and affect ectopic root formation and normal cotyledon development [94]. In poplar, PpnGRF5-1 can reduce the expression level of cytokinin oxidase/dehydrogenase 1 (PpnCKX1), which leads to the accumulation of cytokinin and, thus, promotes the proliferation and formation of meristematic tissue during leaf development [95].

To evaluate the role of GRF and GIF genes in the genetic transformation of plants, a GRF4–GIF1 chimera was overexpressed in wheat, using the maize ubiquitin promoter [34] (Table 1). This approach achieved an almost 8-fold increase in the transformation efficiency in the wheat variety Kronos, significantly higher than that achieved through expressing GRF4 or GIF1 alone. Similarly, the GRF4–GIF1 chimera has also successfully enhanced the transformation and regeneration efficiency in other wheat varieties and the rice variety Kitaake [34]. Its application in sorghum has increased the transformation efficiency to nearly eight times that of the original method, without any significant growth defects [96]. Moreover, the overexpression of GRF5 in Arabidopsis increases the chlorophyll content and delays leaf senescence [97]. The application of GRF5 and its homologs in beet and maize also significantly improve the genetic transformation efficiency, especially the outstanding transformation results achieved by using the ZmGRF5-LIKE1 gene in maize. The application of the GRF5 gene in soybean shows the potential to enhance bud proliferation, but decreases root formation and negatively impacts whole plant regeneration, which thus needs to be further optimized [35]. The role of GRF5 in enhancing genetic transformation efficiency is significant for sugar beet (Beta vulgaris), canola (Brassica napus), and sunflower (Helianthus annuus), with the most pronounced effect on sugar beet [35]. Overall, GRF4–GIF1, GRF5, and their homologs can effectively enhance the regeneration of monocotyledonous plant species (Table 1). However, the specific pathways and molecular mechanisms involved remain undefined.

2.9. REF1 Peptide Regulates the Process of Plant Regeneration

Recent research has identified a novel regeneration factor, REGENERATION FACTOR1 (REF1), derived from the SPR9 gene in tomato (Solanum lycopersicum) [45]. SPR9 encodes a precursor protein for the small peptide SlPep, a member of the plant elicitor peptide (Pep) family, consisting of 23 amino acids. Plant elicitor peptides (Peps), such as SlPep, function as damage-associated molecular patterns (DAMPs) that play critical roles in the plant immune system [98,99,100]. These peptides are released in response to damage, activating defense mechanisms by binding to specific receptors on plant cells known as Pep receptors (PEPRs). This binding triggers a cascade of defense responses that enhance the resistance to pathogens, including bacteria, fungi, and herbivores [100].

Beyond their role in immunity, Peps have also been found to influence plant regeneration processes. The study demonstrated that SPR9 is crucial for regeneration in tomatoes. Knocking out SPR9 resulted in the loss of wound-induced callus formation and organ regeneration capacity, whereas the overexpression of SPR9 or the exogenous application of the peptide significantly enhanced the plant’s regeneration ability. These findings indicate that SlPep not only functions as a key signaling molecule in immune responses, but also plays a pivotal role in promoting regeneration. Consequently, this peptide has been renamed REGENERATION FACTOR 1 (REF1) to reflect its dual function in both defense and regeneration, underscoring its importance as an endogenous signaling molecule in plant responses to damage and stress. Further research has confirmed that REF1 exerts its effects through binding to the leucine-rich repeat receptor-like kinase PORK1 (PEPR1/2 ORTHOLOG RECEPTOR-LIKE KINASE 1), which serves as its receptor. Upon the recognition of REF1 by PORK1, the expression of the key downstream regulator SlWIND1 is activated (Figure 2). SlWIND1 is crucial for cellular reprogramming, initiating tissue repair and organ regeneration processes (Figure 2). Additionally, SlWIND1 binds to the promoter region of the REF1 precursor gene, enhancing its expression and leading to the production of more REF1 peptides, thereby amplifying the REF1 signal [45].

Importantly, the function of REF1 is conserved across the plant kingdom. REF1 peptides and their receptors are found in nearly all dicots and monocots. The exogenous application of REF1 significantly increased the transformation efficiency of wild tomato species (S. peruvianum and S. habrochaites) by 6 to 12-fold. Similarly, in soybean, the application of GmREF1 improved the transformation efficiency of the Dongnong-50 variety by 2.5-fold, demonstrating its potential to promote gene integration and regeneration in soybean cells. In wheat, TaREF1 was applied to immature embryos, resulting in a 4-fold increase in transformation efficiency in the JM22 variety, highlighting its crucial role in promoting regeneration in Gramineae plants. Similarly, in maize, the expression of ZmREF1 increased the transformation efficiency of the B104 variety by 4-fold. Collectively, these results indicate that REF1 can effectively enhance transformation efficiency across diverse plant species [45] (Table 1), suggesting its broad applicability in the fields of plant biotechnology and bio-breeding.

2.10. Overexpression of LAX1 Enhances Shoot Regeneration Efficiency in Plants

TaLAX1 is a recently identified developmental regulator, whose overexpression has been shown to significantly increase the regeneration efficiency of the wheat genotype Fielder [68]. Prior research has revealed that loss-of-function mutations in TaLAX1 result in a compact spike phenotype [101]. LAX PANICLE1 (OsLAX1) and BARREN STALK1 (ZmBA1), the homologous genes of TaLAX1 in rice and maize, respectively, encode atypical basic helix–loop–helix transcription factors [102,103]. OsLAX1 is critical for the formation of axillary meristems in rice, while zmba1 mutants exhibit unbranched and shortened tassels. However, the involvement of these genes in plant regeneration remains unclear.

Further investigations have demonstrated that the overexpression of TaLAX1-A promotes shoot regeneration across a range of wheat genotypes, including five common wheat varieties (Chinese Spring, Kenong 199, Shannong 28, Aikang 58, and Jimai 22) and two durum wheat varieties (Langdon and Kronos), including those known to be recalcitrant to transformation [68]. RNA-sequencing (RNA-seq) analysis of Chinese Spring calli, conducted five days after the transfer to a shoot-induction medium, revealed that tissues overexpressing TaLAX1-A exhibited upregulation of several key genes, including ETHYLENE RESPONSE FACTOR 115 (ERF115), WIND1, ESR1, PLT3, PLT5, and PLT7. Additionally, endogenous levels of hormones, such as auxin, cytokinin, and jasmonic acid, were significantly elevated in calli overexpressing TaLAX1-A compared to the controls. TaLAX1-A was also found to directly regulate the expression of TaGIF1. These findings suggest that TaLAX1-A may regulate shoot regeneration through a mechanism akin to the TaGRF4–TaGIF1 pathway, indicating a regulatory network involving auxin, cytokinin, jasmonic acid, and related transcription factors, like TaGRFs and TaGIF1 (Figure 2), which are integral to cell division, cell fate transition, and shoot regeneration.

In addition to elucidating the role of TaLAX1 in wheat regeneration, researchers have explored potential applications of its homologous genes in soybean and maize (Table 1) [68]. Notably, the overexpression of GmLAX1 in soybean variety Dongnong-50 resulted in an approximate 1.7-fold increase in regeneration efficiency, highlighting its potential for promoting soybean tissue culture and regeneration. Conversely, the overexpression of ZmBA1 in maize variety B104 led to an approximate 3.4-fold increase in the regeneration efficiency, demonstrating that ZmBA1 significantly enhances cell division and regeneration capabilities in maize [68].

3. Conclusions and Perspectives

The sequential stages of plant regeneration, from explants to whole plant formation, involve various DRs that play distinct roles during each phase. Understanding these stages and the specific contributions of different DRs provides a framework for optimizing genetic transformation processes. Figure 3 illustrates these stages, highlighting how individual DRs contribute to specific phases of plant regeneration, thereby improving the overall efficiency of genetic transformation (Table 1).

At the initial stage of co-cultivation, specific DRs, such as LBD, rZmGOLDEN2, and REF, are crucial for promoting the dedifferentiation of plant cells, ensuring robust callus formation. As the callus develops, DRs like SERK, WIND1, WOX, and PLT, become essential for maintaining embryogenic competence and guiding tissue organization, accelerating somatic embryo formation. Finally, DRs, such as GRF–GIF complexes and LAX1, facilitate shoot regeneration by regulating cell proliferation and auxin gradients, ensuring the development of fully functional plants (Figure 3).

These observations suggest that a strategic, stage-specific application of DRs maybe significantly enhance transformation efficiency by tailoring the combination of DRs to the specific needs of each regeneration stage. This approach may address genotype dependency and increase the success rates of transformation, supporting the development of healthy plants from explants to maturity.

A holistic approach to employing DRs, informed by a deeper understanding of their roles at each stage, can help design transformation protocols adaptable to a wide range of plant species and genotypes. Future research should prioritize optimizing DR expression levels, timing, and refining their combinations, while also identifying novel DRs to enhance transformation efficiency. Integrating these insights with cutting-edge technologies, such as CRISPR-based gene editing, transgenic breeding, and single-cell RNA sequencing, could provide deeper molecular insights, leading to more robust strategies for crop development.

Furthermore, addressing regulatory and safety concerns associated with gene-edited and transgenic plants is crucial. Developing strategies for monitoring gene flow, assessing environmental impacts, and identifying potential health risks, will ensure the responsible application of these technologies. Innovative approaches, like trait stacking, should also be explored to improve complex agricultural traits and address diverse environmental challenges [3,15].

In conclusion, the strategic application of multiple DRs across different stages of plant regeneration, combined with technological advancements, will provide a comprehensive approach to overcoming the current limitations related to plant genetic transformation. This integrated strategy not only enhances our understanding of plant developmental biology, but also offers practical solutions for sustainable agriculture and food security. By addressing both the scientific and regulatory challenges, we can pave the way for more resilient and sustainable agricultural practices.

Author Contributions

Conceptualization, X.A.; methodology, X.A.; formal analysis, Y.J.; investigation, Y.J.; resources, Y.J.; data curation, Y.J., and S.L.; writing—original draft preparation, Y.J.; writing—review and editing, X.A.; visualization, Y.J. and S.L.; supervision, X.A.; project administration, X.A.; funding acquisition, X.A. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

Author Xueli An was employed by the company Beijing Solidwill Sci-Tech Co., Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Figures and Table

Figure 1. Schematic representation of WUS and BBM genes and their roles in enhancing plant genetic transformation. Genes on the green background are from Arabidopsis, those on the yellow background are from maize, those on the blue background are from rice, those on the dark gray background are from cotton (Gossypium), and those on the faint yellow background are from tobacco (Nicotiana tabacum). The light blue font and boxes indicate hormone-related signaling pathways and biological processes, as well as their related genes. The genes above the different plants denote that they have been employed to improve the genetic transformation efficiency in the respective plant species. The co-cultivation medium is primarily used for the Agrobacterium infection process and is not involved in the callus induction in explants. The processes illustrated reflect maize transformation, as an example.

Figure 3. Schematic representation of developmental regulatory factors that play key roles in the different stages of the whole plant regeneration. The co-cultivation medium is primarily used for the Agrobacterium infection process and is not involved in the callus induction in explants. The processes illustrated reflect maize transformation, as an example.

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