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Review Article

Legume Research, volume 45 issue 12 (december 2022) : 1465-1475

Closing the Gap in the “ABC” Model in Legumes: A Review

Manuel Hidalgo1,3, Cynthia Ramos1, Jonathan Vásquez-Regalado2, Gastón Zolla3,*
1Escuela Profesional de Medicina Humana, Universidad Privada Antenor Orrego, Trujillo, Perú.
2Laboratorio de Fisiología molecular de Plantas del Programa de Cereales y Granos nativos, Facultad de Agronomía, Universidad Nacional Agraria La Molina, Lima 12, Perú.
3Programa Doctoral en Ciencias e Ingeniería Biológicas, Universidad Nacional Agraria La Molina, Lima 12, Perú.

  • Submitted21-04-2022|

  • Accepted19-07-2022|

  • First Online 18-08-2022|

  • doi 10.18805/LRF-694

Cite article:- Hidalgo Manuel, Ramos Cynthia, Vásquez-Regalado Jonathan, Zolla Gastón (2022). Closing the Gap in the “ABC” Model in Legumes: A Review . Legume Research. 45(12): 1465-1475. doi: 10.18805/LRF-694.

ABSTRACT

From the ancestral bisexual flower (BC model) with radial symmetry to Fabaceae flower with bilateral symmetry and a keel petal, it is critical to understand ABC model because high seed yield and food safety depend on flower bud development. Thus, we summarize the information of the genetic mechanism that explains the identity of the floral organs for Sophoreae, Phaseoleae, Dalbergieae and Genisteae tribes. Moreover, we examine the role of non-coding RNAs on floral development at Cajaninae subtribe, Dalbergieae and Genisteae tribes.

INTRODUCTION

Flowers are reproductive organs organized in whorls, that play an essential role in reproduction and yield (Pawar and Rana 2019; Lyngdoh et al., 2018). The genetic study of Arabidopsis thaliana and Antirrhinum majus mutants led to the proposition of the ABC model of flower development (Alvarez-Buylla et al., 2010), which explains the identity of floral whorls being controlled by three classes of genes (A, B and C). Function A only specifies the identity of the sepals; the identity of the petals is controlled by functions A and B; the identity of the stamens is controlled by functions B and C and function C, specifies the identity of the carpels (Soltis et al., 2007; Fig 1). Thus, ABC model and its variations apply to a wide range of gymnosperm (Soltis et al., 2007) and angiosperm species (Irish, 2017). Amongst them, the Fabaceae comprise an affordable source of protein (Jukanti et al., 2017) and minerals for a large proportion of rural populations in the world (Jayalaxmi et al., 2016) and under a context of climate change and a need for food security, their contribution is recognized (FAO, 2021). No data have been published on Fabaceae flower evolution but their diversification started approximately 60 million years ago and the most important clades separated some 50 million years ago (Lavin, 2005). The Fabaceae family was reorganized into six subfamilies, comprising c. 19 000 species (LPWG, 2017). Among them, Medicago truncatula and Cicer arietinum belong to the Trifoleae and Cicereae Tribes, respectively and the ABC model in these species has been studied in detail (Weller and Macknight 2018).
 

Fig 1: ABC model and floral organ identity in Arabidopsis thaliana


 
The aim of this review is to scrutinize the current state of knowledge on “ABC” model at Sophoreae, Phaseoleae, Dalbergieae and Genisteae tribes. Moreover, we examine the role of non-coding RNAs on floral development at Cajaninae subtribe, Dalbergieae and Genisteae tribes.
 
Sophoreae tribe
 
Sophoreae includes approximately 122 species in 14 genera. It is an early-branched Papilionid, often regarded as “primitive” or “basal”, alongside the Swartzieae tribe (Cardoso et al., 2013). Within this tribe, the genus Sophora comprises approximately 50 species (Song et al., 2008). This genus has a variation in the order of development of floral organs, differing from the standard sequential pattern of sepals, petals, stamens and carpels (Tucker 2006). In Sophora tetraptera and within the subfamily Papilionoideae, the variations include a precocious carpel initiation, delayed petal development and late development with interrupted floral organ development (Song et al., 2008). Also, the developmental order is acropetal among whorls and unidirectional from the abaxial side in the whorls of sepals, petals and stamens (Benlloch et al., 2009). This unusual pattern of initiation and development of the floral organs in S. tetraptera is interesting because it suggests that the expression of ABC genes varies according to the initiation, differentiation and development of different types of floral organs (Song et al., 2008). Indeed, the sequence analysis of the putative floral identity genes of S. tetraptera suggests that StLFY, StAP1, StPI and StAG are homologues to LFY/FLO, AP1/SQUA, PI/GLO and AG/PLE for Arabidopsis and Antirrhinum, respectively (Chanderbali et al., 2010). In addition, Southern blot analyses have revealed that there is a single copy of StAP1, StPI and StAG genes in the S. tetraptera genome and two copies of StLFY (Song et al., 2008).
 
In S. tetraptera, the expression of class A gene StAP1 is strictly limited to floral primordia during floral development and to sepals and petals after floral differentiation (Song et al., 2008). Meanwhile, the expression of StPI, a class B homolog gene, is limited to the petals and stamens; with the homolog of the class C gene, StAG, being expressed in stamens, carpels and seeds (Song et al., 2008). These expression patterns are completely consistent with the defined functions of these genes in Arabidopsis and Antirrhinum (Song et al., 2008). Even though the same genes appear to regulate the flowering process in Sophoreae, the sequential pattern of gene expression has been demonstrated to differ from that of Arabidopsis and Antirrhinum on which the ABC model is based (Song et al., 2008).
Song et al., (2008) have suggested that the ABC genes could also be required during the later stages of flower development. This is supported by the findings in Arabidopsis, in which AG appears to be functionally redundant with SHATTERPROOF (SHP) and SEEDSTICK (STK) (Song et al., 2008). However, it has to be considered that the role of AG in the development of Arabidopsis fruit has not yet been fully described. In species such as Impatiens balsamina, the homologous gene IbAG, is expressed in the floral meristem until the ovule production, not being expressed afterwards (Ordidge et al., 2005). Thus, in S. tetraptera, in which the floral identity genes: StAP1, StPI and StAG show low initial expression levels that increase only after the onset of differentiation of floral organs, it has been proposed that these genes could work as the main barrier for the differentiation of floral organs (Song et al., 2008).
 
Phaseoleae tribe
 
Cajaninae subtribe
 
Pigeonpea [Cajanus cajan (L.) Millsp.] belongs to Cajaninae subtribe and it was domesticated in India no earlier than 3,500 years ago (Kassa et al., 2012). Moreover, it has many wild relatives such as C. scarabaeoides, C. sericeus, C. acutifolius and C. albicans (Khoury et al., 2015) (Table 1). Summarizes the 13 homologous genes for the ABC model in C. cajan. Related to the ABCDE model proposed by Theißen et al., (2016), STK has not been identified. On the other hand, Kumar et al., (2021) were able to report only one copy of the FLC and SVP genes, while three paralogs of SOC1were found in the C. cajan genome. CcMADS1.5 is one paralog of SOC1 and it was found to be missing in C. scarabaeoides, C. platycarpus and C. cajanifolius. Finally, Das et al., (2020) were able to report long non-coding RNAs (lncRNAs) and miRNAs during the process of flower development in C. scarabaeoides.
 

Table 1: Cajanus cajan ABC homologues genes.


 
 
Glyciniae subtribe
 
Glycine max and Glycine soja belong to the Glyciniae subtribe. In regards to the ABCDE model proposed by Theißen et al., (2016), a total of 12 MADS box genes were identified as homologs for G. max and G. soja (Table 2). As in other species AP1 is in charge of the development of petals and sepals, while AP3 and PI are involved in that of petals and stamens and Class C AG is involved in the formation of stamens, carpels and ovules. Regarding Class D, SHP1 and SHP2 are involved in the development of ovules, While Class E, homologs SEP1, SEP2, SEP3 and SEP4 have also been (Vasquez-Regalado, 2021). In addition, AP2 and some genes of the floral transition process were identified (Table 2). This data is in agreement with the study of Jung et al., (2012), who also identified WUS, LFY and SPL3 genes. On the other hand, Chi et al., (2011) were able to isolate and characterize GmAP1, which is specifically expressed in sepals and petals. In addition, Machado et al., (2020) identified two genes similar to AG and three genes similar to PI. According to Chi et al., (2017), GmAGL1 is expressed in carpel and its overexpression causes carpel loss. On the other hand, GsLFY showed a high expression in sepals and stamens but having a weak expression in petals and carpels (Guo et al., 2017). On the other hand, Huang et al., (2009), state that GmSEP1 is possibly involved in the development of petals. Finally, GmMADS28, a class E homolog, can control the number of floral organs and petal identity, producing stamen sterility when it is ectopically expressed (Huang et al., 2014). Furthermore, chicken toes-like leaf and petalody flower is a novel and critical pleiotropic regulator of leaf and flower development (Zhao et al., 2017).
 

Table 2: Glycine spp. homologues genes for ABC model.


 
Phaseolinae subtribe
 
The information on the genetic mechanism that explains the identity of the floral organs is scarce in Vigna and Phaseolus. However, 13 and 11 homologs were found for classes A, B, C, D and E, respectively (Theiben et al., 2016) as is detailed in Table 3. Lin et al., (2020) also described VrSE1 in V. radiata, which belongs to class C, modulating cell division in petals and cell expansion in style. On the other hand, integrative genes such as SOC1 and FUL that work as promoters flower transition (Torti and Fornara, 2012). Furthermore, Squamosa Promoter Binding protien-like 8 and SPL9 are able to modulate the expression of SEP3 and MADS 32 (Gou et al., 2019).
 

Table 3: Phaseolus vulgaris and Vigna spp. ABC homologues.


 
Dalbergieae tribe
 
Dalbergieae is regarded as basal Papilionoideae subfamily of Fabaceae. Flower development in this taxon shows a deviation from that of other Papilionoideae. Organ inception is principally acropetal, with a precocious carpel inception. The whorls develop in different manners, with a helicoidal initiation in Dalbergia brasiliensis sepals and a lateral stamen development in Pterocarpus rotundifolius. These patterns appear at initiation and late stage in ontogenesis, rather than at mid-stage, which is opposed to the unidirectional order usually seen in Papilionoideae (Klitgaard, 1999). These variations seem to be controlled at a genetic level by genes of the ABC model. Indeed, the genetic studies in Arachis hypogaea have focused on the regulation of pod formation by MADS-box genes (Li et al., 2016). Some of these genes have been cloned by Mei et al., (2005), who states that they are related to flower morphogenesis in A. hypogaea.
 
Regarding Class A, Alyr et al., (2020) have characterized a genomic region involved in pod and seed size reduction, providing insights into the flowering regulation in A. hypogaea. They studied Aradu.DN3DB, a gene that codes for the transcriptional regulator STERILE APETALA-like (SAP), demonstrating that its expression can negatively regulate AG expression in the perianth whorls. In A. thaliana, SAP is required for the maintenance of floral identity acting in a similar manner to AP1, with severe aberrations in inflorescences being caused by its loss of function, leading to sterile flowers with small petals (Byzova et al., 1999). On the other hand, the expression of AP2 has been proved to be significantly increased in response to drought (Dang et al., 2012). Additionally, the expression profile of A. hypogaea studied by Li et al., (2016) showed that SPL proteins are capable of interacting with different coding genes belonging to the MADS-box family. This gene has also been reported to have floral homeotic A function (Theißen et al., 2016).
 
Recently, Vasquez-Regalado (2021) has performed a study in comparative genomics to find orthologs in the flowering pathway among 13 different species of legumes, where the data for ABC model in Arachis is summarized in (Table 4). On the other hand, the AG expression seems to be highly affected by environmental factors. In a study about Ca2+ regulation in A. hypogaea, the expression of AG related gene called MADS transcription factor family was downregulated in plants grown in free-calcium-sufficient treatment (Yang et al., 2017). In A. hypogaea, Kumar and Reddy (1997) identified a single copy of AG homologous that was tissue specific during flower bud formation. These findings support the hypothesis that the AG locus is related to environmental response. In fact, some of its introns are capable of producing non-coding RNAs that are capable of interacting with different targets at a molecular level (Wu et al., 2018).
 
Genisteae tribe
 
In a Lupinus albus population derived from Kiev Mutant and P27174 is found homologs to class A (Lup009441, Lup020693), homologs to class C (AGL8, AGL21, AGL24, AGL38, AGL42, AGL65, AGL80) and homologs to class D (SEP2, SEP3, SEP4); which are related to ABC model (Rychel-Bielska et al., 2021). Moreover, genes from the ABC model have also been found in the genome of L. angustifolius Tanjil cultivar (Hane et al., 2017). With this information, Taylor et al., (2019) have studied insertion and deletion mutations in the regulatory regions of the major flowering gene LanFTc1, a homolog of Arabidopsis FT. They have further identified transcription factor binding site motifs of AGL9 and PI that are expressed during early vegetative growth in L. angustifolius (Taylor et al., 2019). Genes of the ABC model have also been related to the vernalization response in L. angustifolius, including SEP3, SEP4 and AGL15 (Nelson et al., 2017). In addition, Fig 2 shows Arabidopsis homolog genes for class A, B and C. All of these genes, with the exception of AP2, are classified as MADS-box type genes (Theißen et al., 2016) and possibly encode or interact with transcription factors that contain highly conserved DNA domains in Lupinus (Delgado-Benarroch et al., 2009). In addition, L. angustifolius ABC model (Fig 2) is conceptualized under the floral development mechanism proposed by Bouche et al., (2016).
 

Fig 2: Lupinus angustifolius ABC model.


 
Other genes affecting the flowering process in the genus Lupinus have been published. Thus, Rychel-Bielska et al., (2021) reported the presence of homologs for CO, FT, MFT, PIF4, SKIP1 and VIP3 in L. albus. The same FT gene has a homolog (FTc1) responsible for vernalization and it is located at locus Ku in L. luteus (Lichtin et al., 2020). Meanwhile, in L. angustifolius, there is evidence of similar roles for the homolog LanFTc1, which is associated with vernalization response and flowering time (Taylor et al., 2019).
 
Genisteae non coding RNA controlling floral development
 
The ABC genes can interact with plant hormones (Chandler, 2011), transcription factors (Krishnamurthy et al., 2015) and noncoding RNAs (ncRNAs) such as microRNAs (miRNAs) (Luo et al., 2013). These noncoding sequences are capable of regulating processes involved in floral development (Budak et al., 2020). The ncRNAs include two major groups: lncRNAs and small RNAs (sRNAs).
 
The sRNAs include several different types of RNA, including miRNAs and small interference RNA (siRNA). Some miRNA, such as miR172, have been shown to repress the expression of genes belonging to class A of the ABC model of flower development, including AP2, in sepals and petals (Chen, 2004). Besides, it has been demonstrated that some miRNAs and siRNAs can interact with auxin response factor (ARF) in Arabidopsis thaliana (Marín et al., 2010). Glazinska et al., (2019) reported miRNA and siRNA that are involved in flower development in L. luteus. They also reported 46 differential expressed miRNAs that were found while comparing the upper and lower flowers. Furthermore, two lncRNAs are involved in the regulation of FLC (Yamaguchi and Abe 2012).
In L. angustifolius, the transcript rna-XR_002106613.1 reported in PLncDB V2.0 (Jingjing et al., 2021) is homologous to lncRNA EL0144 (AT2G46192) (Fig 3). According to TAIR (Berardini et al., 2015), this transcript is expressed at different levels, in particular sepals, stamens and carpels, which suggests that the expression of this gene could affect functional genes belonging to the ABC model in Lupinus (Fig 3). AT2G46192 has been demonstrated to have differential expression in response to several conditions. Mergner et al., (2020) have reported that this transcript is upregulated in flower pedicels and flowers and is found in carpels and petals Arabidopsis. On the contrary, it is downregulated in Arabidopsis under drought, heat and salinity stress (Di et al., 2014). In particular, its repression is notable in the pollen of Arabidopsis knockout cyclic nucleotide-gated cation channel 16 mutants exposed to heat stress (Rahmati et al., 2018). These findings suggest that besides regulating flower development, lncRNA EL0144 could also be involved in abiotic stress responses.
 

Fig 3: Non-coding RNA in Lupinus floral development.

CONCLUSION

Based on the results of this review, key genes for the molecular control of ABC model in Fabaceae are proposed. Moreover, EL0144 (AT2G46192), a non-coding RNA, is involved in the floral development and homologues were found in L. luteus, C. sativus, L. sativa and P. persica. Although they need to be validated, the study of non-coding RNA evolution may uncover important regions and highlight the features that drive their functions. After three decades, it is still critical to understand ABC model because high seed yield and food safety depend on flower bud development. However, there is a question that needs to be answered at the genetic level: Are class A genes, a key step in floral evolution that forced the BC model to create new whorls (sepals and petals) to favor pollination through pollinators and avoid the sexual incompatibility present in several families of angiosperms to consolidate the evolution of mating systems in flowering plants?

ACKNOWLEDGEMENT

The authors would like to thank Mercedes Flores for her comments on flower diagrams and this work was supported by Prociencia (177-2015-FONDECYT) and INNOVATE PERU (451-PNICP-BRI-2014).

CONFLICT OF INTEREST

None.

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