INDETERMINATE DOMAIN Transcription Factors in Crops: Plant Architecture, Disease Resistance, Stress Response, Flowering, and More

Abstract

INDETERMINATE DOMAIN (IDD) genes encode plant-specific transcription factors containing a conserved IDD domain with four zinc finger motifs. Previous studies on Arabidopsis IDDs (AtIDDs) have demonstrated that these genes play roles in diverse physiological and developmental processes, including plant architecture, seed and root development, flowering, stress responses, and hormone signaling. Recent studies have revealed important functions of IDDs from rice and maize, especially in regulating leaf differentiation, which is related to the evolution of C₄ leaves from C₃ leaves. Moreover, IDDs in crops are involved in the regulation of agriculturally important traits, including disease and stress resistance, seed development, and flowering. Thus, IDDs are valuable targets for breeding manipulation. This review explores the role of IDDs in plant development, environmental responses, and evolution, which provides idea for agricultural application.

1. Introduction

Due to recent climate change, reduced availability of water and energy resources, and a growing population, it is urgent to develop high-yield crops that can thrive in areas affected by high temperatures and drought. INDETERMINATE DOMAIN (IDD) genes, which encode plant-specific transcription factors, are emerging as promising target candidates for breeding.

Maize INDETERMINATE 1 (ZmID1), which regulates the transition from vegetative to reproductive growth, was the first characterized IDD gene [1]. Comparative genomic analyses have revealed that it belongs to a highly conserved transcription factor family [2,3]. The IDD gene family encodes transcription factors containing a conserved IDD domain with two canonical C₂H₂ zinc fingers (ZFs) and two C₂HC ZFs in the N-terminal region [1,2]. ZmID1 is localized to the nucleus and binds an 11 bp DNA consensus sequence 5′-TTTTGTC(G/C)(T/C)T/a)T/a)T-3′, which many IDD proteins can bind [3,4,5,6,7,8]. Structural and biochemical analyses have shown that IDDs bind to DNA via ZF1-ZF3 [9].

Bioinformatics analysis has indicated that IDDs arose from a common ancestor of Streptophyta [10]. IDDs duplicated extensively after plants colonized land, resulting in ten lineages. The functions of IDDs have diversified with the evolution of terrestrial plants. Since the emergence of IDD genes in land plants, they have been divided primarily into two lineages: SG5 (including Arabidopsis AtIDD14, 15, and 16) and others. The SG5 lineage exists in all land plants. Although the remaining IDD lineages diversified during the evolution of land plants, the MGP lineage was retained in all land plants [7,10]. Moreover, although the number of IDD genes is similar in monocot and dicot genomes, monocots have a greater number of sequence clusters, most of which are grass-specific [10].

The functions of the IDD genes have mainly been clarified in Arabidopsis. AtIDD14, 15, and 16 cooperatively regulate auxin biosynthesis and transport, resulting in the modulation of aerial organ morphogenesis and gravitropic responses [11,12].

AtIDD2 (GAF1), AtIDD3 (MGP), and other AtIDDs interact with DELLA proteins, which are negative regulators of Gibberellic acid (GA) signaling, to regulate genes involved in GA synthesis (GA3ox1 and GA20ox1) and GA signaling (SCL3) [5,6,13].

AtIDD10 (JKD) and MGP interact with the complex of SCARECRAW (SCR)-SHORT ROOT (SHR), GRAS family transcription factors involved in the radial pattern formation of root ground tissues and regulate target genes including SCR [14,15,16]. Other AtIDDs (AtIDD4, 6, 8 and 9) are also involved in the control of tissue formation in root development [17,18].

Although functional information on IDDs other than Arabidopsis is limited, recent studies have revealed several important functions of IDDs in crops. This review focuses on the biological functions and mechanisms of IDDs in crops. Because the SG5 lineage is somewhat distant from the remaining groups of IDDs [10], these groups are discussed separately.

2. Functions of IDD SG5 Lineage Genes

2.1. Leaf Differentiation

Leaves of C₄ plants usually more efficiently use higher radiation, water, and nitrogen for photosynthesis than those of C₃ plants. Engineering C₄ traits into C₃ crops can substantially increase crop yield, especially under hot and arid conditions [19,20,21]. To achieve this, it is important to understand the molecular mechanisms underlying the development of anatomical traits in C₄ plants.

Two rice IDDs, OsIDD12 and OsIDD13, are involved in regulating venous differentiation [22]. In the early stages of leaf development, cell division in the ground meristem produces either mesophyll cells or vascular initials [23,24]. Parallel venation of leaf veins is a characteristic feature of grasses, and the pattern of venation differs between C₃ and C₄ plants. The leaves of C₄ plants possess high vein density and two photosynthetic cell types associated with C₄ photosynthesis. In both C₃ and C₄ leaves, there are midveins, large lateral veins, and intermediate longitudinal veins. However, C₄ leaves produce an additional file of small longitudinal veins during leaf expansion, resulting in decreased distance between the veins [25,26,27] (Figure 1).

In rice plants, OsSHR1 and OsSHR2 have been shown to act redundantly to promote mesophyll cell identity and to determine the positioning of minor veins [22]. Moreover, OsSHR1 and OsSHR2 promote the development of sclerenchyma cells and repress the differentiation of bulliform cells on the abaxial surfaces of the minor veins [22].

Liu et al. (2023) [22] have shown that OsSHRs interact with OsIDD12 and OsIDD13 to regulate vein patterning in rice plants. Double mutants of OsSHR1 and OsSHR2 (Osshr1, Osshr2) and OsIDD12 and OsIDD13 (Osidd12 Osidd13) show similar phenotypes: reduced mesophyll cell numbers, increased minor vein numbers, reduced lobing of mesophyll cells, the appearance of morphologically distinct minor veins, and thickened cell walls of vascular bundles [22]. These traits support the C₄ anatomy.

OsIDD12 and OsIDD13 bind directly to the IDD-binding sequence located in intron 3 of the rice PIN FORMED5c (OsPIN5c) and suppress OsPIN5c expression in combination with OsSHRs (Figure 2a). These results indicate that the SHR-IDD-PIN5c circuit is an ideal target for optimizing anatomical traits in rice to support C₄ biochemistry [22].

In barley, BROAD LEAF1 (HvBLF1) encodes an IDD protein corresponding to OsIDD12 and OsIDD13. Mutations in HvBLF1 form wider but slightly shorter leaves owing to changes in the number of longitudinal cell files [28]. Mutations in maize IDD14 (ZmIDD14) and ZmIDD15, which are orthologs of OsIDD12 and OsIDD13, also show similar leaf phenotype [29]. Therefore, this phenotype is a common feature among Osidd12 Osidd13, Zmidd14 Zmidd15, and Hvblf1 mutants.

2.2. Plant Architecture

Tiller angle, defined as the angle between the main culm and its side tillers, is an important trait for breeding because it affects plant architecture [30]. In cultivated rice, neither a compact nor spread-out plant architecture is beneficial for grain production [31]. Whereas plants with a spread-out architecture can escape diseases that are increased by high humidity, the photosynthetic efficiency and grain yield per unit area decrease because they occupy more space, and shading and lodging are increased. However, whereas compact plants are suitable for high-planting densities, light capture is not efficient, and they are more susceptible to pathogens and insects transmitted by contact. Thus, an appropriate tiller angle is essential for rice production [31]. Besides the tiller angle, lamina inclination (leaf angle) is also an important trait because it affects the amount of light that the leaf can capture for photosynthesis. In lamina inclination, auxin and brassinosteroids (BRs) are involved [32,33,34,35].

The rice mutant of LOOSE PLANT ARCHITECTURE1 (LPA1, OsIDD14) displays a relatively large tiller and leaf angle. LPA1 also affects shoot gravitropism [36]. LPA1 is a functional ortholog of Arabidopsis IDD15 (AtIDD15/SHOOT GRAVITROPIAM5 (SGR5)), which shows reduced gravitropism [12]. In Arabidopsis, AtIDD14, AtIDD15, and AtIDD16 cooperatively regulate the lateral organ morphogenesis and gravitropism via auxin biosynthesis and transport. Further analysis indicated that these IDD proteins promote auxin biosynthesis and transport by regulating spatial auxin accumulation by directly targeting YUCCA5 (YUC5), TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSOS (TAA1), and PIN1 [11].

Liu et al. (2016) showed that LPA1 suppresses auxin signaling by interacting with C-22-hydroxylated or 6-deoxo BRs, which regulate lamina inclination independent of OsBRI1, a BR receptor [37]. They also showed that LPA1 influences the expression of three OsPIN genes (OsPIN1a, PIN1c, and PIN3a) [37] (Figure 2c).

The mutant of maize LPA1 (ZmLPA1, ZmIDD16) shows a phenotype similar to Oslpa1 [38,39].

Mutations in ZmIDD14 and ZmIDD15 decreased the leaf angle by reducing adaxial sclerenchyma thickness and increasing the number of colorless cell layers [29]. Moreover, the double mutant of ZmIDD14 and ZmIDD15 (Zmidd14 Zmidd15) exhibited an asymmetrically smaller auricle, which might be the result of a failure to maintain the expression of LIGULELESS (LG1), the key gene controlling auricle size. ZmIDD14 and ZmIDD15 interact with the INCREASED LEAF INCLINATION1 (ZmILI1), a bHLH-type protein, which binds to the promoter of LG1 to regulate the gene [40] (Figure 2d). The plant architecture of the double mutant Zmidd14 Zmidd15 has an advantage under high-density conditions, and grain yield is increased under high planting density [29].

2.3. Stress Tolerance

To thrive, sessile plants have developed a range of strategies to manage challenging environmental conditions, including drought, salinity, and extreme temperatures.

Although the spread-out phenotype of lpa1 does not seem ideal for breeding, lpa1 shows advantages under drought conditions in dwarf rice [41]. LPA1 is expressed in the pre-vascular cells of leaf primordia and plays a role in the metaxylem enlargement of aerial organs by regulating the genes involved in carbohydrate metabolism and cell enlargement. The narrow metaxylem of lpa1 plants exhibits efficient water use and drought tolerance. Under the genetic background of a semi-dwarf (dense and erect panicle1-ko (dep1-ko) or ebisu dwarf (d2)), lpa1 shows optimal water supply and drought resistance without affecting the grain-filling rate [41].

2.4. Disease Resistance

Since plant diseases reduce crop yield, producing crops that are resistant to pathogens is an important objective in plant breeding. However, the antagonistic relationship between crop yield and immune pathways makes breeding difficult [42].

Sheath blight disease (ShB) is one of the most devastating diseases caused by Rhizoctonia solani in rice [43]. In rice plants, overexpression of OsLPA1 results in resistance to ShB via the activation of PIN1a expression (Figure 2e) [44]. OsLPA1 binds to the OsPIN1 promoter and activates gene expression. Furthermore, 3-indole acetic acid (IAA) treatment and PIN1a overexpression enhances rice resistance to ShB, indicating that auxin enhances resistance to ShB. The levels of pathogen resistance in genes PBZ1 and PR1b were higher in LPA1 or PIN1 overexpression lines and lower in PIN1a RNAi lines than in the WT when plants were infected with Rhizocotonia sloani AG1-1A. These results indicate that LPA1 might control auxin transport via the regulation of PIN1a expression to increase planting density and activate plant defense gene expressions [44].

Subsequent research identified several factors that interact with OsLPA1, OsIDD13, OsIDD3, kinesin-like protein (KLP), and DENSE AND PANICLE 1 (DEP1) [45,46,47]. OsIDD13 and OsIDD3 positively and negatively regulate OsPIN1a expression, respectively [45]. Moreover, OsIDD13, OsIDD3 and OsLPA1 form a transcription factor complex that regulates the OsPIN1a gene. Accordingly, OsIDD13 and OsIDD3 increase and decrease ShB resistance, respectively [45] (Figure 2e).

KLP promotes rice resistance to ShB by enhancing the expression of OsPIN1a together with OsLPA1 [46]. DEP1 negatively regulates rice resistance to ShB by interacting with OsLPA1 and inhibiting the DNA-binding ability of OsLPA1 to reduce OsPIN1a [47] (Figure 2e).

2.5. Fruit Shapes

A genome-wide association study (GWAS) of tomato plants identified the POINTED TIP (PT) gene, which regulates the protuberance of tomato fruit tip [48]. PT encodes the IDD protein that is classified as the SG5 group. A single-nucleotide polymorphism alters histidine (H) to arginine (R) in one of the zinc fingers of the ID domain (referred to as PT^R). In this context, PT^H, with an intact zinc finger, promotes fruit development without a pointed tip by downregulating FRUITFULL2 (FUL2), which modifies auxin transport. Conversely, RT^R is unable to suppress FUL2 expression, leading to the formation of a pointed fruit tip [48] (Figure 2g).

The regulation of auxin synthesis and transport is a shared function among SG5 lineage IDDs in Arabidopsis and grasses [11,22,38]. However, several functions of the SG5 lineage IDDs from Arabidopsis have not been reported in rice or maize.

AtIDD14 regulates starch metabolism by directly activating the promoter of the Qua-Quine Starch (QQS) gene. An alternatively spliced variant of AtIDD14 is induced by cold temperatures, and competitively inhibits AtIDD14 activity by forming a heterodimer, and as a result, starch accumulation is modified in response to cold [49].

AtIDD14 regulates ABA-mediated drought tolerance by promoting ABA sensitivity and ABA-mediated stomatal closure by interacting with the bZIP-type transcription factors ABFs/AREBs [50].

AtIDD16 negatively regulates stomatal initiation by directly binding to and suppressing the SPEECHLESS promoter [51]. Although the combination of OsSCR and OsSHR has been reported to control stomatal development in rice [22,52], the involvement of OsIDDs in this process remains unclear.

3. Function of IDD Genes in Lineages Other than SG5

3.1. Stem Elongation, Secondary Cell Wall

Crop height is an important breeding trait. GAs are crucial for various aspects of plant growth and development, including stem elongation, seed germination, development, and flowering [53]. In the absence of GAs, DELLA proteins repress various GA responses in plants. However, in the presence of GAs, DELLA proteins are degraded through the 26S-proteasome pathway, which eliminates their inhibitory effects, and various GA-dependent responses occur [54].

Rice GROWTH-REGULATING FACTOR1 (OsGRF1) is a GA-responsive gene expressed mainly in the intercalary meristems of rice internodes [55]. The GRF family has been identified as a conserved family of plant-specific transcription factors in various plant species [56,57,58]. GRFs have diverse functions in plant development and growth, including regulation of GA biosynthesis and stem elongation [57,59]. In Arabidopsis and rice, GRFs are the targets of miR396 [60,61,62], a highly conserved microRNA family found in all land plants [63].

OsIDD2 binds directly to the OsmiR396a promoter and enhances its expression by interacting with SLR1 (rice DELLA) [64]. In the absence of GA, OsIDD2 and higher levels of SLR1 promote OsmiR396 expression, resulting in the suppression of OsGRFs. In contrast, the mRNA levels of OsGRFs increase in the presence of GA because of the degradation of SLR1 and reduction in the level of miR396, resulting in stem elongation [64] (Figure 2h).

In addition to dwarfism, OsIDD2 overexpressing plants exhibit fragile leaves and reduced lignin content, which are characteristics commonly observed in plants with defects in secondary cell wall formation [8]. OsIDD2 negatively regulates the transcription of genes involved in lignin biosynthesis, including cinnamyl alcohol dehydrogenase 2 and 3 (CAD2 and CAD3), as well as sucrose metabolism, including sucrose synthase 5 (SUS5). Of these, CAD2 and CAD3 are directly regulated by OsIDD2 [8] (Figure 2h). Collectively, these findings suggest that OsIDD2 plays a negative role in secondary cell wall formation [8] and stem elongation [64].

3.2. Nitrogen Metabolism

The mutant of OsIDD10 exhibits ammonium hypersensitivity during root growth with root tip coiling [65]. OsIDD10 directly activates Ammonium transporter 1:2 (AMT1;2) and Glutamate dehydrogenase2 (GDH2) expression by binding to their promoters and modulating NH₄⁺ uptake in rice, depending on N supply [65] (Figure 2i). In the ammonium-dependent regulation of root growth by OsIDD10, CALCINEURIN B-LIKE INTERACTING PROTEIN KINASE 9 (CIPK9) has been identified as a direct target of OsIDD10 [66] (Figure 2i).

3.3. Seed Development

The cereal endosperm stores nutrients that provide energy for germination and early seedling development and is important for human food, livestock feed, and industrial commodities.

In Maize, the duplicated genes naked endosperm1 (nkd1) and nkd2 encode ZmIDDveg9 and ZmIDD9, respectively. Double mutants of NKD1 and NKD2 show various effects, including multiple layers of peripheral endosperm, opaque and floury endosperm texture, decreased anthocyanin and carotenoid accumulation, decreased kernel dry weight, and occasional vivipary [67,68].

Normal maize has a single aleurone layer. Meanwhile, the naked double mutant produces multiple outer cell layers of partially differentiated cells that occasionally express aleurone identity markers, such as Viviprous1 (VP1) [67,68]. NKD1 and NKD2 directly regulate gene expression, including Opaque2 (O2), VP1, and Prolamin-box-binding factor1 (PBF1), while NKD2 negatively regulates NKD1 expression, indicating feedback regulation [68] (Figure 2j).

Subsequent studies have shown that NKD1, NKD2 and O2 interact to affect endosperm development [69]. These three factors promote starch metabolism, lipid storage, and storage protein accumulation and constrain the hormone response, cell wall organization, and other cellular developmental processes during the transition from cellular development to storage compound accumulation [69].

In Arabidopsis, ectopic expression of AtIDD1/ENHYDROUS (ENY) disrupts seed development and delays endosperm depletion and testa senescence, resulting in an abbreviated maturation program [70].

3.4. Leaf Differentiation

Recent research has revealed that NKDs in functional combination with SCR control the number of mesophyll cells specified between veins in the leaves of C₄ grass [71].

The mutation of SCR genes in maize leads to disruption in inner leaf patterning, including veins that are separated by only one mesophyll cell, an increase in sclerenchyma, and the presence of ectopic bundle sheath cells; however, no phenotypic changes in stomata are observed. In contrast, mutations in SCR in rice show no stomata, but no phenotype in inner leaf patterning [72]. Furthermore, mutations in the SCR gene in Setaria viridis, another C₄ plant, result in a mixed phenotype of maize and rice; veins are separated by only one mesophyll cell and no stomata. Loss of NKD shows no obvious perturbation in leaf development in maize, Setaria, or rice (rice NKD corresponds to OsIDD10). However, scr:nkd mutants in maize and Setaria, but not in rice, exhibit an increased proportion of fused veins with no intervening mesophyll cells [71] (Figure 2b).

These results indicate that the ancestral role of SCR in grass leaves was the patterning of epidermal cell types, and as C₄ grasses evolved, SCR collaborated with NKD to regulate the pattern of inner leaf cell types. Some C₄ species such as Setaria have retained their ancestral function, whereas others such as maize have lost it [71].

3.5. Disease and Stress Resistance

As mentioned above, OsIDD3 negatively regulates the defense against ShB by suppressing auxin signaling and activating BR signaling [45,73]. OsIDD3 expression is induced by inoculation with Rizoctonia solani and exogenous auxins. OsIDD3 overexpressing plants developed a wider tiller angle and exhibit altered shoot gravitropism, whereas the knockout mutants show no visible phenotype. OsIDD3 binds directly to the PIN1b promoter and represses its expression [73].

Moreover, OsIDD3 is directly regulated by ABI3/VP1-like 1 (RAVL1) and positively regulates the expression of BRI1, a BR receptor gene, and D2 and D11, the BR biosynthesis genes, in an indirect manner, resulting in the activation of BR signaling [74] (Figure 2e).

On the other hand, OsIDD3 enhances chilling tolerance by activating the C-repeat binding factor 1 (CBF1) expression by binding to the promoter of CBF1 even though the expression of OsIDD3 is not affected by cold or ABA stimuli [75] (Figure 2k).

OsIDD10 is also involved in pathogen resistance. OsIDD10 interacts with BRASSINAZOLE-RESISTANT1 (BZR1), a key transcription factor in BR signaling and activates AMT1;2 directly [76]. Under light conditions, Phytochrome B (PhyB) interacts with OsIDD10 and BZR1 to inhibit their DNA-binding activities, resulting in reduced AMT1;2 expression. Under dark conditions, OsIDD10 and BZR1 are released from PhyB and enhance NH₄⁺ uptake by activating AMT1;2. The phyB mutant exhibits tolerance to ShB and saline–alkaline stress because of the expression of AMT1;2, which enhances NH₄⁺ uptake, and tolerance to ShB and saline–alkaline stresses is increased. Further experiments have demonstrated that PhyB-OsIDD10-AMT1;2 signaling regulates the saline–alkaline response, whereas the PhyB-BZR1-AMT1;2 pathway modulates ShB resistance [76] (Figure 2f,l).

In contrast, OsIDD10 negatively regulates rice resistance to ShB by interacting with NAC079 to inhibit ethylene biosynthesis and signaling genes [77]. Exogenous ethylene induces the expression of pathogenesis-related genes (PR genes) in rice [78]. Overexpression of the ethylene biosynthesis gene, OsACS2, which encodes 1-amino cyclopropane-1-carboxylic acid synthase, enhances ShB resistance [79]. The OsIDD10 and NAC079 complex directly activates ETR2, a negative regulator of ethylene signaling. CALCINEURIN B-LIKE INTERACTING PROTEIN KINASE 31 (CIPK31) interacts with phosphorylate NAC079 to increase its transcriptional activity. In addition, AMT1 inhibits the expression of OsIDD10 and CIPK31, resulting in activation of the ethylene signaling pathway, which positively regulates ShB resistance [77] (Figure 2f).

Genome-wide characterization of OsIDDs shows that the expressions of most OsIDD genes respond to abiotic stresses, such as low temperature and drought, and plant hormones, such as auxin, GA, and ABA, indicating that many OsIDDs are involved in stress responses [80].

In Arabidopsis, AtIDD4 negatively regulates the basal immune response and pathogen-associated molecular pattern (PAMP)-triggered immunity [81]. AtIDD4 directly binds to and activates the promoter of the SALICYLIC ACID GLUCOSYLTRANSFERASE1 (SAGT1) encoding enzyme, which converts salicylic acid (SA) to the biologically inactive storage forms SAG and SGE [81,82]. According to the classification of IDDs by Prochetto and Reinheimer (2020), ZmNKDs, OsIDD3, and AtIDD4 belong to the same clade [10].

3.6. Flowering

In the plant life cycle, the transition from vegetative to reproductive growth is a crucial event, and it is fine-tuned by both environmental and endogenous factors [83,84]. The timing of rice flowering, or heading date, is a critical agricultural characteristic that affects rice yield and adaptation to various climatic and environmental conditions [85,86].

The first identified IDD was ZmID1, which regulates flowering [1]. ZmID1 is expressed in immature leaves, and its expression is not affected by variations in light, dark, or circadian patterns [87]. ZmID1 regulates the expression of CENTRORADOALIS 8, (ZCN8) encoding FT homologous protein which possesses florigenic activity [88] (Figure 2m). However, whether ZCN8 is directly regulated by ZmID1 has not yet been determined.

In rice, RICE INDETERMINATE1 (RID1)/Early heading date 2 (Ehd2)/OsID1/Ghd10 has been identified as an ortholog of ZmID1 (hereafter referred to as RID1) [89,90,91]. Mutations of RID1 exhibit a never-flowering phenotype. OsIDD4 has been identified as a Suppressor of rid1 (SID1) that rescues the never-flowering phenotype of the rid1 mutant [92]. The sid1 mutant displays a moderately late flowering phenotype. In addition to SID1, OsIDD1 and OsIDD6 have been found to restore rid1 to flowering when overexpressed. These results indicate that these IDDs redundantly regulate rice flowering. Moreover, RID1 and SID1 directly target the promoter regions of Heading date 3a (Hd3a: rice FT) and FLOWERING LOCUS T1 (RFT1) [92].

Recent studies have shown that RID1 interacts with the methyltransferases SET DOMAIN GROUP PROTEIN 722 (SDF722) and SLR1 [93]. Zhang et al. (2022) proposed the following model: When the SLR1 level is high, Hd3a and RFT1 expressions are suppressed because RID1 is inactivated by interacting with SLR1. During rice development, SLR1 levels progressively decrease in young leaves, leading to the reduced suppression of RID1 and SDG722. The RID1 released from SLR1 recruits SDG722 to promote the accumulation of H3K4me3 and H3K36me3 in the chromatin regions of Hd3a and RFT1. As a result, the chromatin states of Hd3a and RFT1 in the newly developed leaves become activated, allowing them to be recognized and activated by upstream flowering genes. The accumulation of sufficient amounts of florigen proteins (Hd3a and RFT) in the shoot apical meristem initiates a shift from the vegetative to the reproductive stage [93] (Figure 2m).

Analysis of the genome-wide binding sites of RID1 reveal that RID1 binds to the TTTGTC motif and significantly enriches the TEOSINTE BRANCHED1, CYCLOIDEA, PCF (TCP), bHLH, and SQUAMOSA PROMOTER BINDING PROTEIN (SBP) binding motifs by interacting with the novel flowering regulators OsTCP11, OsPIL12, and OsSPL14, respectively [93]. ChIP-seq results indicate that RID1 binds to the promoters of several flowering genes, including HD1 (rice CO), GRAIN NUMBER, PLANT HEIGHT AND HEADING DATE (GHD), and so on. Moreover, a novel RID1 target, OsERF#136, which encodes the AP2 transcription factor, has been identified as a flowering repressor. RID1 negatively regulates the expression of OsERF#136, resulting in flower induction [94] (Figure 2m).

Recently, ZmID1 orthologs have been identified in Brachypodium distachyon (BdID1) and Sorghun bicolor (SbID1), and mutations in these genes result in delayed flowering, as in maize and rice, by regulating several flowering genes, including the homologs of FT and CO [95,96]. The orthologs of ZmID1 belong to a grass-specific lineage of IDDs [2,10]

In Arabidopsis, AtIDD8 promotes photoperiodic flowering by directly activating the expression of SUCROSE SYNTHASE4 (SUS4), thus regulating sugar transport and metabolism [97]. Under energy-deprived conditions, the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE1 (SnRK1) is activated [98] and KIN10, the subunits of SnRK1, interact with and phosphorylate two serin residues of AtIDD8 to repress its activity [99].

4. Concluding Remarks and Future Perspectives

Recent studies have revealed several important functions of IDD genes in rice and maize. The functions of IDD genes discussed in this review are summarized in

Table 1. IDD gene functions described in this study.

Gene	ID	Function	Lineages (Based on [10])	References
Rice
OsIDD1	LOC_Os03g10140	Flowering transition	GAF1	[92]
OsIDD2	LOC_Os01g09850	Stem elongation		[64]
		Secondary cell wall structure		[8]
OsIDD3	LOC_Os09g38340	Disease resistance	NKD	[45,73]
		Chilling torelance		[75]
		BR signaling		[74]
		Auxin transport		[73]
OsIDD4 (SID1)	LOC_Os02g45054	Flowering transition	NKD	[92]
OsIDD6	LOC_Os08g44050	Flowering transition	NKD	[92]
OsIDD10 (OsNKD)	LOC_Os04g47860	N metabolism	NKD	[65,66]
		Disease resistance		[76,77]
		Saline alkaline tolerance		[76]
OsIDD12	LOC_Os08g36390	Leaf vein formation	SG5	[22]
OsIDD13	LOC_Os09g27650	Leaf vein formation	SG5	[22]
		Disease resistance		[45]
OsIDD14 (LPA)	LOC_Os03g13400	Leaf and tiller angle formation	SG5	[36,37]
		Disease resistance		[44,45,46,47]
		Auxin transport		[36,37,44,45,46,47]
OsID1 (RID1)	LOC_Os10g28330	Flowering transition	ID1	[89,90,91]
Maize
ZmIDDveg9 (NKD1)/Zmveg9 (NKD2)		Seed (endosperm) deveopment	NKD	[67,68]
		Leaf vein formation		[71]
ZmIDD14/ZmIDD15		Leaf angle formation/Auricle development	SG5	[29]
		Leaf formation		[29]
ZmIDD16 (ZmLPA1)		Leaf and tiller angle formation	SG5	[38,39]
ZmID1		Flowering transition	ID1	[1,87]
Barley
BROAD LEAF1 (HvBLF1)		Leaf and tiller angle formation	SG5	[28]
Tomato
PT		Fruit shapes	SG5	[48]

. It is particularly interesting that OsIDD12 and OsIDD13 regulate vein density by interacting with OsSHR, indicating that these transcription factors contributed to the evolution of C₄ plants from C₃ plants [22]. However, ZmIDD14 and 15, which correspond to OsIDD12 and 13, are involved in the regulation of the leaf angle [28].

Instead, the functional combination of NKD and ZmSCR was involved in the regulation of the venation patterns in the inner leaf tissues of C₄ plants, but not in those of C₃ plants [71]. Although both rice and maize belong to Poaceae family, some functions of IDDs vary between C₃ rice and C₄ maize plants, indicating IDDs have changed their functions during evolution from C₃ to C₄ plants.

Although some functions are conserved between Arabidopsis (dicot) and rice (monocot), many functions have been reported only in either Arabidopsis or rice. In Arabidopsis, IDDs have been extensively analyzed in root development, GA synthesis, and signaling [27,100]. However, there are few reports on these functions in rice or maize IDDs. Further analyses will reveal the undiscovered functions of IDDs in rice and maize.

The function of IDDs in crops other than rice and maize remain largely unknown. Recent genome-wide studies have identified IDD genes in several plants and analyzed their structure and expression [101,102,103]. Further detailed functional analyses of these genes and IDD genes in several other crops are required.

As outlined in this review, IDD genes regulate agriculturally important traits, indicating that they are valuable targets for genetic modifications to optimize plant growth and development under various environmental conditions.