Angiosperms can be divided into chloroembryophytes and leucoembryophytes, depending on the presence or absence of chlorophyll (Chl) in the embryo, respectively (Puthur et al., 2013; Smolikova and Medvedev, 2016). Some plant species such as Arabidopsis (A. thaliana) produce chloroembryos, which have photochemically active chloroplasts capable of producing assimilates that are further converted into reserve biopolymers (Simkin et al., 2020). Grass species, such as rice (Oryza sativa), are unable to produce Chl during embryo development. To the best of our knowledge, it remains completely unclear what determines the ability to biosynthesize Chl in plant embryo. However, studies have identified several genes that contribute to Chl degradation for chloroembryos, the mutation of which can lead to a stay-green phenotype in mature seeds such as Mendel’s green pea (Sato et al., 2007; Delmas et al., 2013; Wang et al., 2018; Li et al., 2017; Thomas and Ougham, 2014).

Golden 2-Like (GLK) genes encode GARP-type transcription factors (TFs), which are key components regulating chloroplast development and Chl biosynthesis in plants (Rossini et al., 2001; Fitter et al., 2002; Nakamura et al., 2009). GLK can recognize the CCAATC cis-element of the Chl biosynthesis- and photosynthesis-associated nuclear genes to trigger their expression (Waters et al., 2009). The G-box (CACGTG) is also enriched in the GLK-targeted genes in Arabidopsis, possibly due to GLK being able to interact with certain G-box binding factors (Tamai et al., 2002). A genetic study showed that GLK activates Chl biosynthesis in roots, in a manner dependent on the G-box binding TF Elongated Hypocotyl 5 (HY5) (Kobayashi et al., 2012).

There are two copies of GLK in the rice genome, designated as OsGLK1 and OsGLK2 (Fitter et al., 2002). They redundantly regulate a set of genes, such as rice Chlorophyllide A Oxygenase (OsCAO) and Protochlorophyllide Oxidoreductase A (OsPORA) responsible for Chl biosynthesis, and Light Harvesting Complex B1 (OsLHCB1) and OsLHCB4 responsible for photosynthesis (Nakamura et al., 2009; Wang et al., 2013; Sakuraba et al., 2017). OsGLK1 overexpression in rice leads to green calli and chloroplast development in the vascular bundles (Nakamura et al., 2009; Wang et al., 2017). Organelle development in rice vascular sheath cells is induced by ectopically expressed maize (Zea mays) GLK genes, mimicking a key step in the evolutionary transition from C3 to C4 plants (Wang et al., 2017). In accordance with this, the ectopic expression of maize GLKs in rice can boost biomass and grain yield by facilitating chloroplast development and photosynthesis (Li et al., 2020; Yeh et al., 2022). Moreover, the overexpression of maize GLKs in calli was shown to improve the ability of rice and maize to regenerate (Luo et al., 2023). A recent study found that OsGLK1 also participates in tapetum plastid development and programmed cell death, consequently affecting pollen fertility in rice (Zheng et al., 2022). The findings indicate that GLK plays multiple roles in relation of plant development.

Leafy Cotyledon 1 (LEC1), a member of the nuclear factor Y (NF-Y) TF family, is a central regulator controlling many aspects of seed development, such as Chl accumulation in the embryo (Meinke et al., 1994; Pelletier et al., 2017). LEC1 can also act as a pioneer TF to regulate flowering by reprogramming the embryonic chromatin state (Tao et al., 2017). Previous studies have reported that lec1 mutants have paler green embryos than wild-type (WT) at maturation in Arabidopsis (Meinke et al., 1994; West et al., 1994). LEC1 transcriptionally regulates the expression of genes that encode light-reaction components of photosystems I and II, as well as the expression of genes involved in chloroplast biogenesis in Arabidopsis and soybean embryos (Pelletier et al., 2017; Jo et al., 2020). These findings suggest that LEC1 is important for photosynthesis and chloroplast development during seed development. However, the underlying molecular mechanisms remain largely unclear.

It is still a mystery why plant species such as rice cannot synthesize chlorophyll in embryos, while species such as Arabidopsis can. There are two LEC1 homologs, OsNF-YB7 and OsNF-YB9, encoded by the rice genome (Zhiguo et al., 2018). OsNF-YB7 is restricted to the embryo, and defective OsNF-YB7 may result in seed lethality (Niu et al., 2021b; Zhang and Xue, 2013). Here, we found that OsNF-YB7 acts as a key inhibitor of Chl biosynthesis in rice embryo. It inactivates the transactivation activity of OsGLK1, at multiple regulatory layers, to inhibit Chl accumulation in the embryo of rice, explaining the achlorophyllous embryo produced in rice.

In crops such as soybean and canola, the presence of green embryos is considered as a valuable trait due to its association with increased photosynthetic capacity, which consequently promotes fatty acid biosynthesis (Ruuska et al., 2004). This highlights the potential value of the green embryo. Nevertheless, the degradation of chlorophyll in mature seeds is necessary to prevent adverse effects on seed viability and meal quality (Chung et al., 2006).

By surveying 1094 species from 666 genera and 182 families, Yakovlev and Zhukova, 1980 found that 428 angiosperms produce embryos with the presence of chlorophyll. Seeds with chlorophyllous embryo are scattered throughout the angiosperms and have evolved in many unrelated groups, but they are more prevalent in non-endospermous seeds (Dahlgren, 1980). Currently, the evolutionary force driving the divergence of chloroembryophytes and leucoembryophytes remains largely unknown. Embryo photosynthesis contributes a large amount of oxygen to fuel energy-generating pathways in seed (Simkin et al., 2020). The presence of chlorophyll in the embryo facilitates photosynthesis at early developmental stages, potentially leading to improved seedling growth and vigor (Smolikova and Medvedev, 2016). In many chloroembryophytes, such as Arabidopsis, the embryo occupies a large proportion of the seed. From an evolutionary perspective, the presence of chlorophyll in the embryo may promote adaptation in such chloroembryophytes, as more reserves can be accumulated in the seed through active photosynthesis, better supporting the embryo development and subsequent seedling growth (Sela et al., 2020). On the other hand, some leucoembryophytes, such as rice, have a persistent endosperm rich in storage reserves to nourish embryo development (Liu et al., 2022). The acquisition of the ability to accumulate chlorophyll in the embryo is not necessary in such species. Although chlorophyllous embryos are rare among the ‘primitive’ angiosperm superorders, they are observed in some (but not all) Nymphaeales species that are surrounded by some amount of endosperm (Yakovlev and Zhukova, 1980). As there is a paucity of knowledge regarding the evolution of chlorophyllous embryos, further comprehensive studies are necessary.

Some algae and gymnosperm species have evolved an ability to synthesize Chl in the dark (Myers, 1940; Ranade et al., 2019; Bogorad, 1950). However, it has remained largely unclear whether access to light accounts for the induction of chloroembryos (Dahlgren, 1980; Periasamy and Vivekanandan, 1981; Liu et al., 2017). Here, we found that removing the tissues covering an embryo failed to produce chlorophyllous embryos in the WT; however, light avoidance inhibited Chl accumulation in osnf-yb7 embryos (Figure 1—figure supplement 2A–H). These results suggest that light is necessary but insufficient to trigger chloroplast biogenesis in rice. Because light itself does not induce Chl accumulation in rice embryo (Figure 1—figure supplement 2I–L), we inferred that there are intrinsic cues to repress chloroplast development in rice embryo. However, to the best of our knowledge, the underlying mechanism that determines an embryo’s ability to synthesize Chl is completely unknown. Here, we showed that OsNF-YB7, a LEC1 homolog of rice, acts as an inhibitor to repress Chl accumulation in the embryo. In line with this, a recent independent study also showed that the OsNF-YB7 null mutant accumulates Chl in the embryo, although the cause of this remains unresolved (Guo et al., 2022).

Several TFs involved in chloroplast development and photomorphogenesis in rice have been identified (Nakamura et al., 2009; Li et al., 2019; Bai et al., 2019; Hudson et al., 2013). Interestingly, we found that many of them were upregulated in the osnf-yb7 embryos. For example, OsGLK1 was shown to be the most activated (Figure 3A and B). Our genetic and biochemical evidence suggests that OsGLK1 is involved in the OsNF-YB7-mediated repression of Chl biosynthesis in rice embryo. OsGLK1 overexpression mimicked the chloroembryo phenotype in WT, while knockout of OsGLK1 and OsGLK2, simultaneously, suppressed Chl accumulation in osnf-yb7 embryo (Figure 4A–G). The biochemical experiments suggested that OsNF-YB7 associates with the promoter of OsGLK1, in vivo, to transcriptionally inactivate OsGLK1 (Figure 3D–F), indicating that OsGLK1 is a downstream target of OsNF-YB7. However, OsNF-YB7 alone failed to bind to the promoter of OsGLK1 in vitro (Figure 3—figure supplement 1), presumably due to some as-yet-unidentified TFs being recruited by OsNF-YB7, assisting in recognizing OsGLK1 for transcriptional regulation. An NF-Y TF complex usually consists of three subunits (NF-YA/B/C) in order to exert its function (Laloum et al., 2013). NF-YA is responsible for DNA binding, while NF-YB and NF-YC are primarily responsible for transactivation (Chaves-Sanjuan et al., 2021; Gnesutta et al., 2017). OsNF-YB7 possibly forms a heterotrimer with NF-YA and NF-YC in the embryo to recognize OsGLK1. In addition, previous studies showed that Arabidopsis LEC1 can interact with different TFs for developmental regulation (Huang et al., 2015b; Yamamoto et al., 2009; Fatihi et al., 2016; Boulard et al., 2018; Huang et al., 2015a). Identifying such TFs may reveal how OsNF-YB7 recognizes OsGLK1 in order to exert its function.

OsNF-YB7 could recognize a common set of genes involved in Chl biosynthesis and photosynthesis that are recognized by OsGLK1 (Figure 2E–H and Figure 5—source data 1). The biochemical results suggested that OsNF-YB7 can directly repress OsPORA and OsLHCB4, which are activated by OsGLK1 (Figure 2J, and Figure 5—figure supplement 1). OsNF-YB7 probably hinders OsGLK1 to access the target genes by forming an OsGLK1/OsNF-YB7 heterodimer (Figure 6A–E), or by occupying the motif OsGLK1 recognized in the promoter, given the binding sites of OsGLK1 and OsNF-YB7 are likely overlapped (Figure 5F, Figure 5—figure supplement 3 and Figure 5—source data 1). The first of these hypotheses is more plausible because, upon co-incubation of OsGLK1 and OsNF-YB7 with the OsPORA promoter in vitro, the shifted band signal of OsGLK1 was substantially decreased (Figure 6G), indicating that the protein-protein interactions overwhelm the protein-DNA interactions. Thus, when OsNF-YB7 is expressed, it interacts with OsGLK1, then OsGLK1 is less available to activate downstream targets. The findings suggested that OsNF-YB7 plays a dual role in regulating Chl biosynthesis in rice embryo: first, it represses the downstream genes, achieved via its function as a transcriptional inactivator; second, OsNF-YB7 can interact with OsGLKs to disturb their abilities to transactivate genes related to Chl biosynthesis and photosynthesis (Figure 6—figure supplement 2). In addition to OsNF-YB7, a recent study showed that Deep Green Panicle 1, a plant-specific protein with a conserved TIGR01589 domain, can interact with OsGLKs to suppress OsGLK-mediated transcription (Zhang et al., 2021b). The findings suggested that, as the central regulator responsible for chloroplast development, GLK is tightly regulated at the post-translational level to fine-tune Chl biosynthesis in plants.

Previous studies suggested that Arabidopsis LEC1 is a positive regulator of Chl biosynthesis (Pelletier et al., 2017), given that the mature embryos of lec1 were paler than the WT (Meinke, 1992; West et al., 1994). However, the null mutation of OsNF-YB7 activated Chl biosynthesis, implying that the LEC1-type gene acts as a negative regulator in rice. By surveying the literature, we noted that Meinke reported that the cotyledons of the lec1 mutant remained green unusually late in development (Meinke, 1992). Although there was no significant difference in Chl content upon using whole seeds for quantification, Parcy et al. did observe that the tip of lec1 cotyledons accumulated more Chl (Parcy et al., 1997). Moreover, the lec1;abi3 double mutant embryos produced much more Chl than the abi3 single mutant (Parcy et al., 1997). Pelletier et al. recently reported that a cluster of LEC1 targets is enriched in genes related to photosynthesis and chloroplast development, and many of which are down-regulated in the embryo of lec1 (Pelletier et al., 2017); however, we noticed that in their dataset, the photosynthesis and Chl biosynthesis related genes were more strikingly enriched in the up-regulated genes of lec1, at either the mature green or postmature green stage. These observations challenge the concept that LEC1 positively regulates Chl biosynthesis and photosynthesis in Arabidopsis. Most studies in Arabidopsis have emphasized the importance of LEC1 in embryo development at the maturation stage. However, LEC1 is activated within 24 hr after fertilization (Lotan et al., 1998), but its role in the early embryo developmental stages for Chl biosynthesis is still unknown. Previously, we have expressed OsNF-YB7 in the lec1-1 background, driven by the native promoter of Arabidopsis LEC1 (Niu et al., 2021b). Given that OsNF-YB7 could rescue embryo morphogenesis defects in Arabidopsis (Niu et al., 2021b), we postulated that OsNF-YB7 in rice plays a similar role to that of LEC1 in Arabidopsis. In order to ascertain whether LEC1 can fully restore osnf-yb7, it is necessary to ectopically express LEC1 driven by the native OsNF-YB7 promoter in the osnf-yb7 background in the future, due to the possibility of functional divergence between the genes with regard to the regulation of chlorophyll biosynthesis in the embryo. It would also be worthwhile to carry out similar tests in other grass organisms to better understand the regulatory mechanism in rice.

In addition to producing chlorophyllous embryo, the osnf-yb7 mutants display an array of developmental defects, including abnormal embryogenesis, reduced dormancy, and desiccation intolerance, similar to those found in Arabidopsis lec1 mutants (Niu et al., 2021a). Mutation of osglk1 and osglk2 in osnf-yb7 could recover the chloroembyo phenotype, but did not alleviate the other embryo defects (Figure 4D–G). The findings suggest that OsGLKs specifically function in Chl biosynthesis, but that OsNF-YB7 is responsible for many aspects of embryo development. In agreement with this, the number of OsNF-YB7-targeted genes is far greater than that of OsGLK-targeted genes, and the DEGs in osnf-yb7 embryo is far greater than that in OsGLK1-OX embryo (Figure 4H and Figure 5E). The mechanisms underlying the OsNF-YB7-regulated multiple embryo developmental processes require further investigation.

Sequencing data have been deposited in NCBI BioProject under the accession code PRJNA998591.

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Author details

1. Zongju Yang

   1. Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/ Zhongshan Biological Breeding Laboratory, Agricultural College of Yangzhou University, Yangzhou, China
   2. Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops/ Key Laboratory of Plant Functional Genomics of the Ministry of Education, Agricultural College of Yangzhou University, Yangzhou, China

   Contribution

   Conceptualization, Data curation, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing - original draft

   Contributed equally with

   Tianqi Bai and Zhiguo E

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4700-049X

2. Tianqi Bai

   Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/ Zhongshan Biological Breeding Laboratory, Agricultural College of Yangzhou University, Yangzhou, China

   Contribution

   Validation, Investigation, Visualization, Methodology

   Contributed equally with

   Zongju Yang and Zhiguo E

   Competing interests

   No competing interests declared

3. Zhiguo E

   State Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou, China

   Contribution

   Software, Investigation

   Contributed equally with

   Zongju Yang and Tianqi Bai

   Competing interests

   No competing interests declared

4. Baixiao Niu

   1. Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/ Zhongshan Biological Breeding Laboratory, Agricultural College of Yangzhou University, Yangzhou, China
   2. Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops/ Key Laboratory of Plant Functional Genomics of the Ministry of Education, Agricultural College of Yangzhou University, Yangzhou, China

   Contribution

   Investigation

   Competing interests

   No competing interests declared

5. Chen Chen

   1. Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/ Zhongshan Biological Breeding Laboratory, Agricultural College of Yangzhou University, Yangzhou, China
   2. Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops/ Key Laboratory of Plant Functional Genomics of the Ministry of Education, Agricultural College of Yangzhou University, Yangzhou, China

   Contribution

   Conceptualization, Supervision, Funding acquisition, Visualization, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   chenchen@yzu.edu.cn

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9748-3111

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