Updated role of ABA in seed maturation, dormancy, and germination

Abstract

Background: Seed is vital for plant survival and dispersion, however, its development and germination are influenced by various internal and external factors. Abscisic acid (ABA) is one of the most important phytohormones that influence seed development and germination. Until now, impressive progresses in ABA metabolism and signaling pathways during seed development and germination have been achieved. At the molecular level, ABA biosynthesis, degradation, and signaling genes were identified to play important roles in seed development and germination. Additionally, the crosstalk between ABA and other hormones such as gibberellins (GA), ethylene (ET), Brassinolide (BR), and auxin also play critical roles. Although these studies explored some actions and mechanisms by which ABA-related factors regulate seed morphogenesis, dormancy, and germination, the complete network of ABA in seed traits is still unclear.

Aim of review: Presently, seed faces challenges in survival and viability. Due to the vital positive roles in dormancy induction and maintenance, as well as a vibrant negative role in the seed germination of ABA, there is a need to understand the mechanisms of various ABA regulators that are involved in seed dormancy and germination with the updated knowledge and draw a better network for the underlying mechanisms of the ABA, which would advance the understanding and artificial modification of the seed vigor and longevity regulation.

Key scientific concept of review: Here, we review functions and mechanisms of ABA in different seed development stages and seed germination, discuss the current progresses especially on the crosstalk between ABA and other hormones and signaling molecules, address novel points and key challenges (e.g., exploring more regulators, more cofactors involved in the crosstalk between ABA and other phytohormones, and visualization of active ABA in the plant), and outline future perspectives for ABA regulating seed associated traits.

Keywords: Desiccation tolerance; Embryogenesis; Phytohormones; Seed development, Seedling establishment.

Graphical abstract

Fig. 1

Regulation of seed development and dormancy by ABA biosynthesis through the carotenoid pathway started from β-carotene (C40). The complete ABA synthesis process takess place in plastids and cytoplasm where ZEAXANTHIN EPOXIDASE (VPs, ZEP, ABA1/2) converts zeaxanthin into antheraxanthin and all trans-violaxanthin. ABA4 catalyzes the conversion from all-trans-violoxanthin to the all-trans-neoxanthin. The conversion of xanthoxin from 9′-cis-neoxanthin and 9′-cis-violaxanthin is exerted by VP14 and NCEDs (NINE-CIS-EPOXYCAROTENOID DIOXYGENASE), among which the NCEDs display different subcellular localization of plastid or cytoplasm. The oxidation of abscisic aldehyde by AAO3 (ABSCISIC ALDEHYDE OXIDASE3) is responsible for the conversion from abscisic aldehyde into ABA, which in turn induces and maintains seed dormancy. But, it is yet unknown of the factors responsible for the conversion from all-trans-violoxanthin /all-trans-neoxanthin to 9-cis-violoxanthin/9-cis-neoxanthin.

Fig. 2

The ABA signaling pathway is involved in seed development. Left, in the absence of ABA: Receptors PYLs release and activate protein phosphatase 2C (PP2C) such as ABI1/2 and AGH1/3. Downstream SNF1-RELATED PROTEIN KINASE subfamily (SnRK2s) genes are inactivated by active PP2C which leads to premature germination and the non-dormant seed through repression of lots of transcription factors such as ABI1/2/3/4/5 and bZIP67. Right, in the presence of ABA: Receptors PYR/PYL/RCAR bind ABA and PP2C together to inhibit the activity of PP2C, which release the activity of SnRK2s and downstream transcription factors such as ABI3 by protein phosphorylation, then regulate downstream genes SGR1/2 function to mediate seed de-greening process. Additionally, the active LAFL (ABI3, FUS3, LEC1, and LEC2) network by ABA along with WRI1 regulates the At2S3 gene; an active bZIP22 function downstream of SnRK2s to promote gene transcription of 27-kD γ-zein for protein reserve accumulation in the seed. Along with seed de-greening and storage product accumulation, SnRK2s function upstream of ABI3/5 and ABFs to regulate LEAs and HSPs that are pivotal for desiccation tolerance. In other branches, DOG1 also plays a role upstream of ABI3/5/ABFs as well as functions as a repressor of PP2Cs (AHG1/3) to involve seed desiccation tolerance acquirement. In combination, all key ABA signaling components (SnRK2s, ABI3, ABI4, ABI5, ZmbZIP22, bZIP67, and ABFs) are involved in storage product accumulation, de-greening, and desiccation tolerance with different function pathways to provide a mature and dormant seed. Letters “P” and “T” in the color circles indicate the two manners of protein phosphorylation and gene transcription regulation, respectively. Activated and repressive effects are shown by arrows and bars, respectively.

Fig. 3

The function of ABA in seed germination and seedling establishment. Left, Seed completes germination successfully through degradation of active ABA into PA (phaseic acid) and DPA (dihydrophaseic acid)/DPAG with CYP707As regulated by REF6 and phaseic acid reductase (ABH2 and GT) respectively. During germination and seedling establishment, the core ABA signaling component SnRK2s and downstream ABI3/4/5 are activated or repressed by many factors directly or indirectly to promote seed germination and seedling establishment. For example, RAV1 and BASS2 bind to the ABI4 promoter to inhibit ABI4 expression, while MYB96 promotes ABI4 expression through binding to its promoter. A Casein Kinase 2 promotes ABI4 expression indirectly. Furthermore, ANAC060 transcription is activated directly by ABI4 through binding to its promoter to enhance post-germination. Several BTB-A2 proteins can impair SnRK2.3 stability to act as negative regulators of ABA signaling. NRT1.2 is identified as an ABA transporter to regulate downstream factors ABI1-ABI5, RAB18, etc. positively to mediate germination and seedling development. Further, some negative factors such as SUN24, UGT74E2, FOF2, and VQs regulate seed germination and seedling development through repressing ABI3-, ABI5-mediated ABA pathway. Activated and repressive effects are shown by arrows and bars, respectively.

Fig. 4

The interplay of ABA and other phytohormones (GA, ET, SA, BR, and Auxin) signaling in the regulation of seed germination and post-germination growth. ABA crosstalks with other phytohormones either by affecting their biosynthesis or by interfering with their signaling pathways during germination and post-germination growth. Among these, the interaction between ABA and GA is most studied and important. FUS3 and ABI4 play more vital roles to mediate the antagonism between ABA and GA. SA was found to regulate the content of ABA negatively and GA positively, respectively in seed germination. Both two factors LFL and CHO1 were showed inhibition to GA synthesis to involve seed germination regulation. After that, some downstream factors of GA such as SPY, SNY, SLY, SIZ, RGL2, etc. display different functions in the crosstalk between GA and ABA. Both SIZ and RGL2 can repress and promote ABI5, respectively. Besides, RGL2 can be degraded by CSN1 and regulate ABI5 together with an NF-CY factor. ABA-mediating ABI3, ABI5, and RGL2 regulate MFT by establishing a negative feedback loop to modulate the ABA and GA antagonism, in which, MFT also inhibits ABI5. A study indicated that auxin stimulates ABI3 expression through ARF10 and ARF16 indirectly, which connects the ABA and auxin in seed germination regulation. In some ways, ABA inhibits ACO and ACS to influence ethylene synthesis negatively. Meantime, ETR1/2 and histone deacetylation cofactors SNL1/2 mediate the antagonism between the ABA and ethylene to involve seed germination, in which some ERF factors are involved. BR promotes seed germination as well as inhibits BIN2, which interacts with ABI5 and positively regulates ABA responses during seed germination and post-germination. Activated and repressive effects are shown by arrows and bars, respectively.