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Review Article

A Short Review on the Identification of ABCDE Genes in Monocot Plants

Suchilkumar Soorya ¹, Thacheril Sukumaran Swapna ¹, Kalluvettankuzhy Krishnan Nair Sabu ²*

1 Department of Botany, University of Kerala Kariavattom, Thiruvananthapuram 695581, India

2 Biotechnology and Bioinformatics Division, Jawaharlal Nehru Tropical Botanic Garden and Research Institute, Palode, Thiruvananthapuram 695562, India

Article history:

Submission April 2022 Revised June 2022 Accepted August 2022

ABSTRACT

One of the most important divisions in the plant kingdom is the monocotyledon division of angiosperms. More than 60,000 monocot spp. have been identified, the major- ity of which are economically important, such as the Poaceae, Orchidaceae, Are- caceae, Liliaceae, and certain other families. The involvement of the ABCDE model of floral organ determination during flower development is a growing area of research in the field of molecular biology due to the diversity in the floral morphology of monocots. The MADS-box gene family is a large molecular transcript family that helps identifies specific proteins involved in floral development. It is classified into several classes based on its function. The review aimed to evaluate the significance of ABCDE genes for floral development and subsequent organ identification, which have been discovered in a range of monocot plants, as well as the functions of these genes in determining the sex of dioecious plants. We sought to summarise the MADS- box gene responsible for flower initiation and floral whorl differentiation reported in economically valuable monocotyledonous plants.

Keywords: ABCDE model, Dioecious, Floral organ identity, MADS-box gene,Mono- cots

*Corresponding author:

E-mail: [email protected]

Introduction

Flowers are planted reproductive organs and modified shoots that are functionally and physi- cally distinct from nearly every other aspect of the vegetative shoot system. Flower initiation is regu- lated primarily by external factors such as sun- shine and temperature and internal factors such as the appropriate functioning of certain genes involved in floral organ development. As a result of the influence of these two stimuli, changes in cell destiny occurred within the shoot apical meristem, which is responsible for the shift from the shoot system to blossom initiation. To present, researchers studying gene mutations in flower development have discovered that the unique roles of distinct genes are involved in the production of floral whorls. Floral identity, cadastral, and meristem identity genes are the three genes that influence flower growth [1]. Floral identity genes, for exam- ple, AGAMOUS, APETALA, PISTILLATA, etc., are directly responsible for the development of flo-

ral organs. These genes were discovered through mutation experiments in floral identity genes in Arabidopsis that resulted in variations in floral organ MADS-box genes that account for the major- ity of organ identity genes in flowers.

The MADS-box gene family is named after four members: MINICHROMOSOME MAINTE- NANCE1 from Saccharomyces cerevisiae AG (AGAMOUS) from Arabidopsis thaliana, DEF (DEFICIENS) from Antirrhinum majus, and SRF (SERUM RESPONSE FACTOR) from Homo sapi- ens [2–5]. The MADS-box genes encode a DNA binding protein structure known as a MADS domain, which is a highly conserved 50-60 amino acid sequence at the N terminus. These domain proteins cause transcription factors to be attached to the CArG boxes (CC [A/T] GG) sequence motif in DNA [6]. According to studies on MADS-box domain phylogenetic relationships, MADS-box genes are categorized into two types: type I and

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JTLS | Journal of Tropical Life Science 424 Volume 12 | Number 3 | September | 2022

type II [7]. In Arabidopsis thaliana, sixty-two type one and forty-six type two genes have been discovered and described. Type I genes are classified into three subgroups based on structural characteristics, Mα, Mβ, and Mγ while type II genes are separated into two subgroups, MIKCc and MIKC*, which are known as the M-type gene [4, 8, 9]. In yeast and animals, type I MADS genes correspond to a conserved portion of SRF-like protein domain, while type II group genes encode genes like MEF2. However, according to recent findings, MIKC genes are only found in plants. Type II genes have been found in plants. In plants, type II genes have a strongly conserved MEF2-like MADS-box, weakly conserved intervening domain (I), keratin-like domain (K), and variable C domain [10, 11].

According to a recent study, the MADS-box family plays an important role in many areas of developmental cycles, including the formation of flowers and fruits, male and female gametophytes, embryos and seeds, and so on. Some MADS-box genes in angiosperms have homeotic functions.

Although not all MADS-box genes are homeotic, they can act as meristem identity genes. ABC model was a new approach towards flower initiation proposed in 1991 to make clear the ability of homeotic genes in the organ identity of a flower

suggests that the organ identity in each flower whorls is determined by a unique companies activity of three organ identity genes [12]. The ABC model was subsequently expanded to the ABCDE model [3–5, 13–15].

According to this model, A-Class genes are involved in the sepal formation and, together with class B genes, regulate the formation of petals.

Stamen development is mediated by class B genes in conjunction with class C genes, while carpel formation is determined solely by class C genes.

D-class genes regulate ovule development, while Class E genes are found throughout the meristem, where flowers develop, and are critical for normal floral organ production [16]. In this model, class A contains genes APETALA1, APETALA2, and FRUITFULL; class B contains PISTILLATA and APETALA3; class C has AGAMOUS, and it is the first identified MADS-box genes from Arabidop- sis thaliana and DEFICIANS from Antirrhinum majus; class D includes SEEDSTICK and SHAT- TERPROOF; class E includes SEPPALATA genes (Figure 1) [17–19].

The studies on the contribution of ABCDE genes in flower development reported that the floral whorls originated in the following order: stamens, carpels, petals, and sepals. Furthermore, the ABCDE and AGL6 genes may have appeared in

Figure 1. Modified ABCDE model. APETALA1 [AP1], APETALA3 [AP3], PISTILLATA [PI], AGAMOUS [AG], SEEDSTICK (STK), SHATTERPROOF1 and 2 (SHP1 and SHP2) [20].

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this order: Genes starting with B, AGL6, E, C, D and the A genes [21]. AGL6 genes are important in floral development in monocots and eudicots [21]. In a recent study based on the functional divergence of the MADS-box gene state, the ABCDE model was used to determine the roles of ABCDE and AGL6 genes in developing floral or- gans. AGL6 genes in monocots and eudicots have been found to play an important role in floral development [21]. MADS-box genes display diver- sification in Arabidopsis and Antirrhinum floral homeotic gene mutation studies. These genes are major controllers of floral diversity in dicot and monocot plants. As a result, it’s critical to figure out how these genes control floral organ development in flowering plants, which has been studied extensively in dicot plants. MADS-box genes have recently been discovered in several monocot plants that are similar to the ABCDE MADS-box

genes found in dicot plants [22]. However, studies into the function of MADS-box genes in monocots are limited. To present, monocot MADS-box gene research has focused on members of the Poaceae and Orchidaceae families. Meanwhile, a literature review reveals that MADS-box gene studies have been carried out on species of the Arecaceae, As- paragaceae, Liliaceae, Commelinaceae, Poaceae, Orchidaceae and other families. We attempted to focus reports in this review on all ABCDE gene research that took place at the floral development of monocot plants in relation to model dicot plants as well as the involvement of MADS-box genes in dioecious plant sex differentiation.

In the current period, the involvement of ABCDE flowering genes in the development of floral organ formation is a hot research topic. Ar- abidopsis thaliana is a popular model plant in higher plants because of its small genome size, ease of mutagenization, and the fact that it is used in most research work. The ABCDE model was

developed based on the study of floral homeotic mutations in Arabidopsis, Antirrhinum, and Petu- nia, which explains the importance of these four classes of floral organ identity genes in determining the four floral whorls such as sepals, petals, stamens, and carpals [5, 23]. The ABCDE genes involved in the floral organ identity of Arabidop- sis are listed in Table 1 [24].

Plants dioecious nature provides a large study area for specific genes involved in male and female reproductive organ development. Most research on the role of floral identity genes has been done in hermaphrodite species. Only a few at- tempts have been made to determine the molecular process that causes plants to be dioecious. Sex organ identification is controlled by class B, class C, and class D-genes, according to recent research on floral organ identity genes in Arabidopsis and other hermaphrodite species [1, 13, 22, 25–29]. B,

C, and D-class genes play a crucial role in sex de- termination in dioecious plants such as Spinacia oleracea, Silene latifolia, Cucumis sativus, and others [13, 22, 27, 29–32]

Class A MADS-box genes

APETALA1, APETALA2, and SQUAMOSA are class A function genes identified in A. thaliana and Antirrhinum sp. of which AP1 encodes MADS-box transcription factor and AP2 is associ- ated with a new class of DNA binding proteins [33]. These genes are responsible for the transition from vegetative to reproductive stage. If any of these genes have a mutation, then the sepals and petals are failed to develop properly. In Arabidop- sis sp., a mutation in AP1 causes the sepals to be- come bracts as well as the development of flower buds at the axils of the modified sepals. Moreover, the flowers of transformed plants do not have pet- als [34]. In Arabidopsis thaliana, AP2 play a role Table.1 ABCDE class MADS-BOX genes and its function

CLASS SUB FAMILY FUNCTIONS

A AP1 and AP2 Promote floral meristems, sepals, petals or lemma/palea identities.

Spikelet/floral meristem identity and lodicule identity.

B AP3 and PI Lodicule and stamen identity

C AG Stamen and carpel identity

D AG- SEEDSTICK, SHATTERPROOF1 and SHAT-

TERPROOF2 Ovule identity.

E SEPALLATA1 (SEP1, formerly known as AGL2),

SEP2 (AGL4), SEP3 (AGL9) or SEP4 (AGL3) FM determinacy and floral organ identity

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in hormone regulation specific to flower development and floral organ identity. Molecular analysis of AP2 gene expression revealed that AP2, along with the help of an unidentified gene, will suppress the activity of the AGAMOUS gene [35].

Monocots are rich with diversity in flowers and inflorescences. Therefore, studying the genes responsible for the variations in floral architecture is of great importance. Recently, homologous of the ABCDE MADS-box genes in dicots have also been found in some monocot species and the ma- jority of this study was done in grass species such as rice, wheat, and maize. But the cDNA of the MADS-box gene was first reported in orchids even though studies have also reported on other economically important monocots such as oil palm, Lilium sp., Asparagus sp., Allium sp., bam- boo, pineapple, Tulipa sp. [27, 28, 36].

Three AP1-like MADS-box genes were dis- covered in the rice genome, such as Os- MADS14/RAP1B, OsMADS15/RAP1A, and Os- MADS18 that are completely generated from FRUITFULL of Arabidopsis instead of AP2. In addition, two AP2-like genes were discovered, which regulate changes in the fate of the spikelet meristem and determine the structure of the inflorescence [34, 37, 38]. Rice has recently been shown to have two genes that are similar to AP2, SUPERNUMERARY BRACKET (SNB) and OsIN- DETERMINATE SPIKELET1 (OsIDS1), both of which are required for lodicule formation [39].

Several studies have led to the role of flowering genes, especially in the ABCDE model of bread wheat (Triticum aestivum). The investigation of pistalloidy in wheat lines revealed that three genes, namely [5, 34, 40], WFUL2, and WFUL3 are orthologous to AP1 genes of rice [13]. These genes do not have class-A activities, but they are linked to the transition from the vegetative to re- productive periods. The wheat Q (TaAP2) gene was shown to be orthologous to AP2 similar genes in Arabidopsis sp. and to be involved in the pro- duction of lodicules in wheat by phylogenetic analysis [34, 40].

Studies in sequence similarity and expression analysis of maize identified an orthologue of the AP1 gene in Arabidopsis sp. named ZAP1. In ad- dition, ZMM4 and ZMM15 are similar to the Os- MADS14 gene of rice and show similarities in the functions of rice OsMADS18 [5, 41]. In situ hy- bridization and expression studies in barley class, A genes resulted that HvBM14, HvBM15, and

HvBM18 are not functionally similar to those of AP1 and SQUA [42]. Even though, these three genes are expressed throughout the development of the inflorescence regardless of tissue or organ.

However, the HvBM18 gene was expressed in all other organs, similar to the rice OsMADS18 gene [5]. PheMADS15, an AP1-like gene, is strongly expressed during flower bud organ differentiation, according to genome wide discovery of MADS- box gene from Moso bamboo (Phyllostachys edu- lis) [43]. MADS genes in bamboo and other mon- ocots have evolutionary links that are identical to genes within the ABCDE model of flower development. BeMADS14, BeMADS15, and BeMADS18 were members of the AP1 family, which is identified from Bambusa edulis [44].

BeMADS14 is similar to OsMADS14. BeMADS15 is similar to ZAP1 in maize and OsMADS15 in rice. BeMADS18 is similar to OsMADS18 from rice [45].

In orchids, OMADS10 is an orthologue to AP1 genes. RT-PCR analysis denoted that the OMADS10 gene is not expressed in the initial stages of flower bud development and is gradually expressed in mature flowers [3, 5, 25, 46–48]. But High expression was also found in the vegetative part, such as leaves. This expression pattern is di- verged from A-class genes in the Arabidopsis sp., Antirrhinum sp., and grass family but is similar to the AP1 orthologue of Lilium sp. named LMADS5 and LMADS6 [36, 46, 49]. Lilium sp. also pos- sesses another class A gene, LMADS7 [5].

LMADS5 and LMADS6 were discovered to have high expression in leaves, stems, and carpels but low expression in other floral whorls. LMADS7 was absent in leaves and any floral whorls but was present in stem and inflorescence meristem. The ABCDE model was used to assess the temporal and spatial expression patterns of several im- portant genes in Allium sativum. According to their expression analysis, the AsAP1 and AsAP2 genes are class A genes found in tepals and carpels [37]. Recent studies in conserved ABCDE MADS-box genes in pineapple have been identified and are homologous to ABCDE floral devel- opment model in Arabidopsis sp., rice, and Antir- rhinum sp.. Two A-class genes were identified from pineapple, AcFUL1 and AcFUL2. AcFUL1 have similarity with FUL-like I rice genes such as OsMADS15 and OsMADS14, and AcFUL2 is sim- ilar to FUL-like II rice genes such as OsMADS18 and OsMADS20 [12].

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The MADS-box gene characterization from oil palm identified 12 genes, of them EgSQUA1, EgSQUA2, and EgSQUA3 which are SQUAMOSA subfamily of Class A genes. RT-PCR analysis re- ported that EgSQUA1 is constantly expressed in developing pistillate and staminate flowers [27, 50]. CsAP1a, CsAP1b, and CsAP1c are three ho- mologous AP1-like genes that were cloned and characterized by the Crocus. They are expressed in both vegetative and floral tissues. Their se- quence similarity reveals AP1-like gene similari- ties; however, this is unable to determine a func- tional involvement for these genes in Crocus [51].

Class B MADS-box genes

Studies in Arabidopsis thaliana suggest that class B function genes determine petal and stamen development [18, 52]. B-class genes are split into two lineages based on evolutionary relationships:

DEF-like lineage and GLO-like lineage. Under the DEF-like and GLO-like lineages, there are two transcripts: AP3-like proteins and PI-like proteins [25, 53]. Many monocots found that there was only a DEF-like gene. So AP3 genes are highly conserved in most of the monocots [5]. There are three B-class MADS-box genes identified from the rice genome. The evolutionary data shows that OsMADS2 and OsMADS4 are members of the GLO-like lineage, and the OsMADS16 gene is un- der the DEF-like lineage. Generally, these discov- eries show that the two PI-like OsMADS4 and Os- MADS2 and the OsMADS16 are AP3-like a gene, B-class genes in rice [5, 38, 39]

In wheat, two B class MADS-box genes were identified and are highly similar to AP3-like genes in rice. WPI1 (wheat PISTILLATA1) and WPI2 are the PI-like genes found in wheat. Based on the phylogenetic analysis, these two genes were orthologous to rice PI-like genes OsMADS4 and OsMADS2. WPI1 and WPI2 are also called TaPI- 1 and TaPI-2/TaAGL26 [5, 34, 40]. Similarly, the AP3 orthologue of Zea mays named SILKY1 is normally expressed during the period of stamen and lodicule development [40, 45]. In maize, B class PI orthologous are ZMM18, ZMM29, and ZMM16 which have similar expression patterns to OsMADS2 and OsMADS4 [40, 54, 55]. These genes expression was observed during the development of the lodicule, stamens, and carpal primordia of male and female inflorescence.

Transcript Profiling of MADS-box genes reveals three B class function genes are expressed in

lodicule and stamen development in barley Inflo- rescence. However, AP3/DEF B-class genes are PI/GLO B-class genes [5, 42, 56]. The bamboo ge- nome contains three B-class proteins such as BeMADS2, and BeMADS4, grouped under the PI family. BeMADS2 showed high similarity with OsMADS2 and maize ZMM2. BeMADS4 is close to OsMADS4, and BeMADS16I s belongs to the family AP3 genes and is similar to OsMADS16 [44].

Orchids have four different clads of DEF-like genes, one of which, OMADS3, has the function of an AP3-like gene but lacks a C-terminal motif, which is unlike any other B-class gene discovered thus far [57]. Three DEF-like genes have been dis- covered in orchids: OMAD5, OMADS12, and OMADS9. The expression of the OMADS5 and OMADS12 genes was detected in the sepals and petals of orchid flowers. OMADS9 is highly ex- pressed in the petals but not in the vegetative or- gans. The only gene similar to GLO in orchids is OMADS8 and the expression was detected in the flower’s root, leaf, and four whorls. The formation of petals and petals requires the presence of at least the OMADS3/8/5 and/or OMADS9 gene and the absence of OMAD5 genes leads to labellum devel- opment [57]. The previous report on B class MADS-box genes in lilies revealed that the LMADS1 gene is functionally equivalent to the AP3 in Arabidopsis, which regulates petal and sta- men development. Two PI-like orthologues were identified from Lilium sp. named LMADS8 and LMADS9 [36, 46]. These two genes have similar expression patterns to AP3 and PI in Arabidopsis and rice OsMADS4 and OsMADS16 genes. AsAP3 and AsPI are the B-function genes found in Allium sativum. AsAP3 and AsPI were found to be highly expressed in the tepal and stamen but not in the carpel, according to the studies [37]. Studies in As- paragus officinalis L. a B functional gene was identified and named as AODEF gene and is closely related to SILKY1 of maize [58].

Phylogenetic analysis and sequence compari- son studies in Alpinia point out that AhMADS5 and AhMADS8 are very much similar to PI and AP3 families. The expression studies detected that Ah- MADS5 and AhMADS8 were present in the apex of the floral primordium and then localized in the common meristem to develop petals, stamen, and labellum [49, 59]. The reports in the pineapple MADS-box gene family suggested that AcPI genes are found in PI-like lineage and AcAP3

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genes in AP3-like lineage. The gene expression analysis in petals, stamens and pistils resulted that AcPI gene has strong expression, whereas AcAP3 did not show any expression in these organs and was moderately expressed in leaf tissues [12].

Recent studies in the identification and characterization of MADS-BOX gene in oil palm re- ported that one gene, EgDEF1 belongs to the sub- family DEFICIENS. EgDEF1 gene was not ex- pressed in male and female inflorescence. In situ hybridization resulted in the EgDEF1 gene being detected in staminoid cells and the centre of the carpels. In oil palm, two GLOBOSA-like genes were identified and named EgGLO1 and EgGLO2.

EgGLO2 transcript expression was detected in the development stages of male and female inflorescence. In situ hybridization studies reported that the EgGLO2 gene was concentrated in sepals and petals in the mature pistillate flower of oil palm and a strong signal is found in stamens of the staminate flower [27]. According to research on the development of Crocus flowers identified, AP3-like CsatAP3/DEF gene and CsatPI/GLO gene are involved in the transition of sepals to petals [60].

Class C MADS-box gene

The class C gene is required for the normal development of a flower’s stamens and carpels.

AGAMOUS (AG) and SHATTERPROOF1 and 2 (SHP 1 AND 2) are two types of MADS-box genes found in A.thaliana. Typically, AG genes in A.tha- liana play a major role in stamen and carpel devel- opment, as well as floral meristem determination.

These genes are alone found in carpels and in com- bination with the B class gene located in stamens [61]. Genes in the Class C family appear to be an- tagonistic to those in the Class A family. Accord- ing to MADS-box gene studies in the rice genome, there are two genes, OSMADS3 and OSMADS58, which are closely linked and belong to the AG subfamily [62].

In wheat, WAG1 and WAG2 (wheat AGA- MOUS 1 and 2) C-class genes are orthologs of the rice AGAMOUS gene [34]. The expression level of these genes is low in the initial stages of floral primordia and high in the developed floral organs. C- class MADS-box genes WAG1 and WAG2 are spe- cifically called TaAG-1 and TaAG-2/TaAGL39 [34, 63]. There are two AGAMOUS paralogs in maize ZAG1, ZMM2 and ZMM23, an orthologue of rice C-class function genes OsMADS58, and

OsMADS3, respectively. In situ hybridization and RNA blot analysis showed that expression of ZMM2 was detected in primordial stamens and carpels. The expression of ZAG1 was found in an- ther [55]. Barley contains two C-class function genes, namely HvMADS3 and HvMADS58. Both genes are expressed in lodicule and are similar to TaAG-1 and TaAG-2 wheat genes but not to C class function genes of maize [56]. Bamboo BeMADS3 and BeMADS58 were primarily ex- pressed in the floral bud and then subsequently in the anthers and pistils, particularly with high expression levels in the pistils. These findings sup- port the key role of C class genes forming the stamen and carpel [44].

The AGAMOUS clad of orchids has two genes of different functions, of which the OMADS4 gene is c class function gene. The expression pattern of OMADS4 is similar to the AG gene in Arabidopsis which is expressed in the stamen, stigma, and ovule [64]. Several C-class function genes were identified from other orchid species. For example, P. equestris, Phalaenopsis sp. These species’ flo- ral buds and mature flowers show the expression of PeMADS1, PhalAG1, CeMADS1, and OMADS4 genes grouped under the class C genes family [19, 48]. DcOAG1 and DthyrAG1 are AG orthologs of Dendrobium crumenatum, and Den- drobium thyrsiflorum are expressed in all floral or- gans except stamens and carpels [3, 19, 25, 48].

Oncidium is another orchid having the C-class function gene OMADS4 is homologous to LMADS10 of Lilium longiflorum expressed in sta- mens and carpels [46]. LLAG1 is an AG homolog of Lilium sp. exclusively expressed in stamens and carpels [19, 26, 46]. AsAG is an AG-like gene identified from Allium sativum. Studies reported that the AsAG gene shows the highest expression in stamens and decreases at flower maturity [14, 37]. Characterization of MADS-box transcripts from Alpinia hainanensis revealed that AhMADS6 is homologous to the AG C-class gene of Ara- bidopsis sp., and strongly expressed in stamens and carpels [59]. A recent study reported that AcAG is a C-class function gene found in the pine- apple’s male and female reproductive parts, strongly expressed in stamens and ovules [12, 14].

EgAG1 and EgAG2 are AG subfamily genes found in oil palm. The sequence and expression pattern similarity suggested that these genes are pa- ralogues to EgGLO1 and EgGLO2. EgAG2 genes

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were strongly expressed in the ovule [27]. Isola- tion and characterization of C-class genes in Cro- cus revealed the presence of AG1 genes named CsatAG1 in the inner reproductive whorl of the flower and not in the tepals [60].

Class D function genes

Class D genes are first identified in Petunia termed as FLORAL BINDING PROTEIN 7 (FBP 7) and FBP11. These two genes control ovule identity [65]. The Arabidopsis sp. class D gene is represented by SEEDSTICK, which is similar to FBP7 and FBP11 expressed explicitly in develop- ing ovule [66]. MADS-box transcription factors are important components of the genetic network that regulates flower and fruit growth. Class D contains AGAMOUS-like genes involved in the development of fruits [66]. The expression analysis and protein-protein interaction studies of the D- class MADS-box gene in the rice genome have re- ported OsMADS13 and OsMADS21 genes speci- fying ovule development [5, 40]. OsMADS21 is strongly expressed in kernel development [34, 40].

From the wheat genome, five genes were iden- tified and named as TaAGL2, TaAGL9, TaAGL31, TaAG-3A, and TaAG-3B. These genes are orthol- ogous to rice D class function gene OsMADS13 and Arabidopsis SEEDSTICK, so they were re- named WSTK (Wheat SEEDSTICK) [34, 63].

TaAG-4, closely related to OsMADS21, has weak expression in stamens and is highly expressed in the ovule [5, 63]. ZMM1 and ZAG2 have been identified as class D function genes in maize.

ZAG1 is an ovule-specific gene, and the expres- sion is restricted to developing the ovule and the inner carpels [40, 63]. BeMADS13 and BeMADS21 are AG-series D class genes that are expressed in most of the flowers and are localized in the pistils. Gene functions in ovule identity determination and floral meristem determination are consistent with the expression pattern of class D genes [44]. D-class genes in Lilium sp. have one gene LMADS2. It was highly expressed in carpels and very specific to the ovule [46]. HvMADS13 and HvMADS21 are the D class genes found in barley. Studies on the role of HvMADS13 and HvMADS21 genes indicated that they are ex- pressed during carpal development [56].

LMADS2 and LMADS10 together form a het- erodimer, and they can also form a homodimer [36, 46]. In the temporal and spatial expression studies in Allium sativum, AsSTK was a D-class

gene found to be highly expressed in the carpel [37]. A phylogenetic study revealed that AVAG2 belongs to the AG gene family’s D-lineage in As- paragus [67]. In Orchidaceae, DOAG2 is a D class function gene identified from a member of the or- chid family Dendrobium sp. DOAG1 and DOAG2 are reproductive organ identity genes, especially in ovule development [68]. Several D-class genes are identified from other orchid species, such as DthyrAG2 from Dendrobium thyrsiflorum, Phalaenopsis equestris have PeMADS7 gene, PhalAG2 from Phalaenopsis hybrid, OMADS2 and OitaSTK from Oncidium and Orchis italic re- spectively [19, 48]. Studies in identifying organ identity genes in the pineapple reveal that AcAGL11a, AcAGL11b, and AcAGL11c are mem- bers of D-class function genes expressed explicitly in the development stages of the flower [12].

Class E function genes

In Arabidopsis, the class E family consisted of four genes SEPALLATA1 (SEP1), SEP2, SEP3, and SEP5 [69]. These genes interact with ABCD class genes during flower development. Based on the previous studies, the E-class genes in Poaceae are classified into different clads, the LOFSEP and the SEP clade and AGL6-like gene [16]. Os- MADS24 and OsMADS45 are rice orthologs of the SEP gene of Arabidopsis sp., showing similar ex- pression patterns, interactive properties, and high sequence similarity. OsMADS1/LEAFY HULL STERILE 1 (LHS1), OsMADS5/OSM5, and Os- MADS34/PANICLE PHYTOMER2 (PAP2) are in- cluded in the LOFSEP clade [34]. These genes are inflorescence and spikelet meristem identity genes. In rice, AGL6 clade contains two genes, Os- MADS17 and OsMADS6/MOSAIC FLORAL OR- GANS 1 (MFO1) [34, 40]. Both genes are floral organ identity in function [12, 29].

In wheat, E-class genes are grouped under three clads SEP, LOFSEP, and AGL6 clades.

TaMADS1, TaAGL16, TaAGL28, and TaAGL30 genes were included in SEP (WSEP) clade [40].

WSEP gene activities are found in forming lodi- cules, stamens and carpels [34, 40, 63]. TaMADS1 is orthologous to the OsMADS8/24 gene of rice.

The LOFSEP clade includes eight genes from wheat named TaAGL3, 5, 8, 24, 27, 34, and WLHS1. LEAFY HULL STERILE 1 (WLHS1) is orthologous to rice E-class gene OsMADS1/LHS1 [40]. They are highly expressed in lodicule, lemma, palea, and glumes while weak expression

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in stamen and carpels. TaAGL6 and TaMADS37 are AGL6 clade genes, and their function is un- known. Ten E-class genes were identified from maize and grouped into three clades. ZMM6, ZMM7, and ZMM27 are grouped in the SEP clade.

ZMM3, 8, 14, 24, and 31 are LOFSEP clad genes, and the AGL6 clade contains two genes (ZAG3 and 5) [40]. ZMM3, ZMM8, and ZMM14 genes are ho- mologous to OsMADS1. ZMM14 gene expression was strong in carpal primordia than in other organs [70]. ZMM6 is a SEP3 lineage gene found in maize detected in all floret organs during inflorescence development and was highly expressed during kernel development [40, 70]. HvBM1 is otherwise known as the BM7 gene found in barley and iden- tified as an E-class gene expressed throughout flower development but not present in anther [42].

BeMADS1, BeMADS5, BeMADS7, BeMADS8, and BeMADS34 were the E-class genes in the SEP lineage in bamboo. The AGL6 lineage was found to include BeMADS6 [44]. Studies reported that BeMADS1 was shown to be expressed throughout the flower’s development.

In Orchidaceae, E-class genes were identified from a few species, such as Dendrobium sp., Phalaenopsis sp., and Oncidium sp. DcSEP1 gene detected in sepal, petal, and lip of Dendrobium crumenatum, DOMADS1 and DOMADS3 were expressed shoot apical meristem in maturing flowers, indicating that role of these genes in the transition of vegetative to the reproductive stage in Dendrobium grex [44]. Four SEP-like genes were identified and cloned from Phalaenopsis named PeSEP1, PeSEP2, PeSEP3, and PeSEP4. They are expressed in all floral whorls during flower development [43, 64]. Two E-class genes were identi- fied from Lilium sp., LMADS3 and LMADS4.

LMADS3 is an orthologue of SEP3 and expression was similar to that of the OsMADS1-like gene and detected in all four floral whorls but absent in leaves. LMADS4 is orthologue to SEP1/2, ex- pressed in leaf, inflorescence meristem, and all floral whorls [71]. In Allium sativum AsSEP1, three were significantly expressed in garlic’s re- productive and vegetative floral parts. AsSEP1, three may function as floral organ identity genes in garlic since their expression patterns are similar to SEP1, three genes in petaloid monocots as D- class genes [37].

Recent studies in bananas reported three E class genes under SEP clade named MaMADS1 and MaMADS2 homologous to RIN-MADS ripen-

ing gene of tomato. These genes are highly expressed during fruit development [72]. Pineapple SEP clade contains two genes; AcSEP1 and AcSEP3 are orthologs to AcAGL9 in Arabidopsis and OsMADS7/8 in rice [12]. This transcript was highly expressed in all floral organs except petals.

EgAGL2-1, EgAGL2-2, EgAGL2-3, EgAGL2-4, and EgAGL2-5 are MADS-box proteins come un- der the SEPALLATA subfamily. The spatial ex- pression pattern revealed that these genes are involved in developing petals, ovule, stamen, and perianth [27, 50].

Conclusion

MADS-box genes are an important tool for studying floral structure development because of their relevance in forming floral structures and subsequent morphogenesis. They provide important information on the expression patterns of genes involved in floral reproductive organ production, such as stamens and carpels. This review pointed out the importance of class C and D genes, which may be helpful in the determination of sex in monocot and dicot dioecious plants. Due to its complex function throughout organ development, evolutionary relationships suggest that comparing E-class genes to other ABCD class genes is com- plicated. The findings above aid in understanding the role of the MADS-box gene in floral organ identity, which leads to the identification of target genes for crop improvement and has opened up a vast space for researchers to learn more about ABCDE models. MADS-box genes were also con- sidered to be important regulators in a wide range of plant biological processes. This research im- proves the floral organ evolution model, which may be used to analyze the origins of floral organs and MADS-box genes.

Acknowledgments

We thank the Department of Botany, Univer- sity of Kerala, Kariavattom and Department of Bi- otechnology and Bioinformatics, Jawaharlal Nehru Tropical Botanic Garden and Research In- stitute, Palode, for providing facilities. We also thank lab members for their discussion and com- ments on the manuscript. Gratefully acknowledge UGC for providing a research fellowship to Soorya.S.

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