ABSTRACT
As a highly developed tissue, maize endosperm accumulates nutrients abundantly and supports embryo development. In a recent study, we constructed a regulatory network centered around Opaque11 (O11). This network unified cellular development, nutrient metabolism and stress responses during endosperm development. Here we discuss the evidences that O11 might have a regulatory role in cold stress response during seed development. Furthermore, we discuss the functional divergence between maize O11 and its Arabidopsis orthologue ZHOUPI, which might explain some of the differences in endosperm development between monocotyledonous and dicotyledonous seeds.
KEYWORDS: Maize, endosperm development, nutrient metabolism, regulatory network, cold stress response, ZHOUPI
As a product of double fertilization, the triploid maize endosperm provides nutrients and signals to the embryo during the development processes. Unlike the endosperm in the seeds of dicotyledonous species (such as Arabidopsis), which is absorbed by the cotyledons during the course of development,1 maize has persistent endosperm that accumulated nutrients abundantly until maturation. The development of maize endosperm mainly have two phases: the early patterning and differentiation stage (coenocytic, cellularization and differentiation), and the latter kernel-filling stage (storage starch and protein accumulation).1-3 For the past few years, a few regulators in maize endosperm development or/and nutrient reserve accumulation have been identified and studied through genetic and molecular analysis, such as Naked endosperm 1 (NKD1) and NKD2, which regulate both endosperm cell patterning and differentiation as well as resource reserve deposition4,5 Opaque2, positively regulates nearly all zein genes.6-8 However, a regulatory link between the endosperm development and the nutrient reserve accumulation is still missing.
Seed development is an environment sensitive process that is very vulnerable to abiotic stresses. Cold stress as one of the most significant abiotic stresses of agricultural plants affects both plant development and yield.9,10 In Arabidopsis, INDUCER OF CBF EXPRESSION 1 (ICE1)11,12 was identified as an upstream regulator of the CBFs/DREB1 genes13 in the cold response pathway. Interestingly, ICE1 was also reported as a key regulator in stomatal development,14 suggesting the bifunctional roles of ICE1 in regulating both environmental adaptation and developmental processes.
O11 links endosperm development and nutrient metabolism
In a recent study, we found that Opaque11 (O11) as an endosperm-specific bHLH transcriptional facor (TF), coordinates cellular development and nutrient metabolism.15 In the aspect of regulating endosperm development, O11 directly regulates the known key TFs in maize endosperm (NKDs, ZmDof3)4,5,16 and the ortholog of a key molecular switch in plant development,17-19 ZmYODA. In the aspect of regulating endosperm nutrient metabolism, O11 directly regulates not only the well-known TFs in nutrient storage regulation, such as O2 and prolamin-box binding factor (PBF), but also multiple carbohydrate metabolic enzymes.15 Combined with the mutant phenotype caused by the absence of O11 protein – significant decreased starch and protein content as well as morphological defects in embryo, it is suggested that O11 plays a coordinated function between cellular development and nutrient metabolism during maize seed development.
O11 is involved in cold stress response
In addition to the roles of O11 in regulating endosperm development and metabolism, multiple lines of evidence suggest that O11 also plays roles in cold stress response. (1) Loss of O11 function in maize kernel caused massive transcriptional changes of stress response genes, and more than half of them were annotated as response to cold stress; (2) A large proportion of stress response genes directly bound by O11 were functionally annotated as response to cold stress; (3) Plants usually accumulate excess of free proline under abiotic stress, such as extreme temperature.20,21 o11 mutant endosperm accumulated an abnormally high free proline content, suggesting that the mutant endosperm might be in a similar state as in abiotic stress; (4) Our data as well as previous studies22,23 showed that O11 has a very close relationship with ZmICE1, the homolog of a master regulator of cold stress response in Arabidopsis.11,12 O11 and ZmICE1 directly interact with each other and share significant portion of direct targets. Moreover, ZmICE1 transcript increased approximately three times due to the absence of O11.15 The exact role of O11 in cold stress response still needs further investigation. It will be interesting to know if O11 enhanced the tolerance of seed under cold stress, or is O11 a stress-induced protein?
Functional divergence of O11 homologs between monocotyledonous and dicotyledonous species
Earlier studies have reported that ZHOUPI (AtZOU) is a pivotal regulator in controlling both endosperm breakdown and embryonic surface formation during Arabidopsis seed development.24-28 Our studies indicated that, O11 as the homologous protein of AtZOU in maize, shows significant differences from AtZOU in protein sequence and subcellular localizoation.15 Here, the previously identified 4 targets of AtZOU23,24,26 were analyzed in maize (Table 1). The orthologs of these 4 genes were identified by BLASTp searching in the NCBI nr (nonredundant protein sequences) database. Then the transcriptional changes of these genes were examined in o11 mutant. None of them had significant transcriptional change in o11 mutant seeds (P<0.05) (Table 1). We also examined the ChIP-Seq data of O11, and none of these genes were bound by O11 in vivo. With all these evidences, we would like to propose that significant functional divergence had been occurred between O11 and AtZOU, whcih might explain the dramatic differences in endosperm during seed development between monocotyledonous and dicotyledonous species.
Table 1.
Transcriptional changes of the homologues of previously identified AtZOU targets in o11 RNA-Seq data15.
| Maize_Gene ID | Description | WT_FPKM | o11_FPKM | Fold change | P-value | Arabidopsis Gene ID | Other name |
|---|---|---|---|---|---|---|---|
| GRMZM2G015708 | GDSL-motif esterase/acyltransferase/lipase | 0.00 | 0.02 | 1605.8 | 1.00 | AT1G71250 | — |
| GRMZM2G026855 | Pectin lyase-like superfamily protein | 14.97 | 13.71 | 0.9 | 1.00 | AT2G43870 | — |
| GRMZM2G045287 | Reversibly glycosylated polypeptide 3 | 7.13 | 6.54 | 0.9 | 1.00 | AT3G08900 | RGP3 |
| GRMZM2G157313 | PA-domain containing subtilase family protein | 0.12 | 0.19 | 1.5 | 1.00 | AT1G62340 | ALE1 |
Funding Statement
National Natural Science Foundation of China 31425019; National key research and development program of china 2016YFD0101003; National Natural Sciences Foundation of China 91635303; National Natural Science Foundation of China (CN) 91335208
Disclosure of potential conflicts of interest
No potential conflicts of interest were disclosed.
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