Rice seed vigor traced to stage-by-stage transcriptional control across the seed life cycle

Rice seed vigor is not a single score on a germination test. In a wide-ranging review published in Plant Molecular Biology, researchers argue that it is a life-cycle trait whose performance after sowing depends on physiological capacity built during seed development, preserved during storage, and reactivated during germination and seedling establishment. Rather than functioning as isolated stage-specific pathways, transcriptional networks coordinate a series of transitions between protection and growth, and the authors contend that this temporal coordination is exactly what molecular breeding for direct-seeded rice must exploit.

The review defines seed vigor as the capacity of a seed lot to germinate rapidly and uniformly, tolerate adverse conditions, and support vigorous seedling establishment. It is related to, but distinct from, viability, dormancy, and longevity: viability is the ability to germinate under favorable conditions, dormancy blocks an otherwise viable seed from germinating, and longevity describes the retention of viability and performance during storage. A seed lot may therefore retain a high final germination percentage while progressively losing germination speed, uniformity, stress tolerance, and field-emergence capacity. Stronger dormancy can reduce pre-harvest sprouting, but it may also delay germination and establishment after sowing, creating a central breeding trade-off.

This life-cycle view matters most for direct-seeded rice, in which seeds are sown directly into puddled soil, dry soil, or standing water and may encounter chilling, salinity, transient water deficit, oxygen limitation, soil crusting, variable burial depth, and weed competition. Rapid emergence shortens the period during which seedlings depend entirely on seed reserves and improves early canopy establishment, but selection for rapid germination may weaken the dormancy needed to prevent pre-harvest sprouting under warm and humid harvest conditions. The authors frame the breeding challenge not as simply accelerating germination, but as achieving the appropriate transition from pre-harvest protection to post-sowing growth.

During grain filling and maturation, transcription factors regulate embryo development, reserve deposition, nutrient transport, cellular protection, and the acquisition of desiccation tolerance, thereby establishing the physiological capacity of the mature seed. In the embryo, the VP1–ABA-responsive bZIP module is a well-characterized system: rice VP1 cooperates with ABA-responsive bZIP proteins such as TRAB1 to activate maturation-associated transcription, while ABA-activated SAPK/SnRK2 kinases phosphorylate TRAB1 and related bZIPs to increase transcriptional activity. These interactions convert rising ABA into a coordinated protective state characterized by LEA accumulation, desiccation tolerance, and suppression of premature germination. Notably, OsVP1 is reused after maturation, subsequently activating Sdr4 to contribute to post-maturation dormancy control, a direct example of one transcription factor operating across successive stages of the seed life cycle.

In the endosperm, OsbZIP58, also known as RISBZ1 or OsSMF1, is a major regulator of reserve deposition, binding promoters of starch-biosynthetic genes and controlling storage-protein programs together with the Dof factor RPBF, which recognizes prolamin boxes. Maternal nutrient supply adds another layer: OsMADS29 controls programmed cell death in the nucellus and nucellar projection, and perturbing its expression disrupts maternal-tissue degeneration, hormone homeostasis, embryo development, and endosperm filling. The review is careful about evidence, however. Regulators such as OsMADS29, RSR1, the OsNF-YB1–OsNF-YC12–bHLH144 network, and OsbZIP60/OPAQUE3 strongly affect grain development, reserve composition, or proteostasis but currently lack direct post-developmental phenotypic evidence for seed vigor, and should be regarded as developmental candidates rather than established vigor regulators.

Several regulators do bridge development and later performance. OsHSFC1b promotes seed weight, size, and vigor through heat-shock and raffinose-family oligosaccharide pathways, while isoaspartyl modification during storage impairs its activity, directly linking developmental protection with subsequent protein damage and ageing. The OsbHLH001–OsTPS8 module is especially informative because a single promoter variant links chalkiness, trehalose-6-phosphate signaling, α-amylase regulation, and seed vigor across indica and japonica backgrounds; unlike a knockout, this allele changes regulatory amplitude while leaving the protein intact. Seed-vigor differences associated with OsTPS8 were supported by germination assays, diverse genetic backgrounds, and soil-based seedling evaluation under controlled environmental conditions, though these experiments did not constitute replicated field-emergence trials.

During storage, dry seeds are metabolically quiescent but chemically active, accumulating lipid peroxidation, protein carbonylation, isoaspartyl formation, nucleic-acid damage, and membrane instability at rates determined by genotype, moisture, oxygen, and temperature. This damage may remain phenotypically silent during dry storage and become evident only after imbibition, when damaged membranes, mitochondria, and repair systems fail to resume metabolism efficiently. The strongest mechanistic evidence for transcriptional control of storage survival centers on the OsbZIP23–PER1A module: overexpression lines showed improved germination after accelerated ageing, knockout lines showed reduced performance, and OsbZIP23 directly binds an ABRE-containing region of the PER1A promoter to activate this 1-Cys peroxiredoxin, linking ABA-associated transcription to peroxide detoxification. Upstream, auxin signaling increases OsbZIP23 transcription through OsARF12, while SAPK1-mediated phosphorylation enhances the activity of the OsbZIP23 protein, so the OsTIR1-OsIAA10-OsARF12 auxin pathway and SAPK1-bZIP23 ABA-associated pathway converge on a regulatory axis that improves seed vigor.

A second longevity branch is controlled by SAG9, a nuclear protein that negatively regulates storability by interacting with several seed-expressed class-E bZIP proteins and partially suppressing their activation of protective targets such as EM1, LEA3, and Rab16A, while leaving PER1A activation largely intact. A nuclear-localization-defective favorable haplotype improves storability while retaining moderate dormancy, making SAG9 a strong example of a deployable natural allele. Beyond these ABA- and auxin-associated pathways, salicylic acid adds another hormone–redox component: multi-omic and genetic analyses of contrasting rice accessions linked SA content, ROS accumulation, and seed survival to a network containing OsNPR1, PP2C30, bZIP03, and bZIP28, which may integrate SA, ABA, and redox regulation during storage. The authors caution that accelerated-ageing assays should not be equated with long-term natural storage, and that a regulator identified through accelerated-ageing assays should be considered a candidate determinant of storability until its effect is reproduced under longer-term natural or commercially relevant storage conditions.

Dormancy itself is treated as a reversible temporal gate. OsVP1 activates Sdr4 through ABA signaling, while OsWRKY29 binds W-boxes in the OsABF1 and OsVP1 promoters, weakening ABA responsiveness and promoting dormancy release. Temperature-dependent variation in dormancy is mediated in part by the antagonistic bHLH factors SD6 and ICE2, which regulate the ABA catabolic gene ABA8OX3 and indirectly affect the biosynthetic gene NCED2 through OsbHLH048. Post-translational control adds further precision: the SDR3.1 locus encodes MODD, which promotes the deactivation and degradation of OsbZIP46, and a natural indel in GF14h alters temperature-dependent germination through an OREB1–OsMFT2 module. At the maturation-to-germination boundary, OsbZIP58 protein stability becomes part of the pre-harvest sprouting regulatory system, because high temperature activates the sugar-sensing kinase OSK3, which phosphorylates OsbZIP58 and promotes its proteasomal degradation; loss of OsbZIP58 reduces RAB16A activation, derepresses OsAmy3D, accelerates starch hydrolysis, and promotes pre-harvest sprouting.

After imbibition, germination proceeds as a controlled metabolic restart in which ABA–GA balance, sugar and energy signaling, reserve mobilization, ROS homeostasis, and cell expansion determine the timing and uniformity of germination. Brassinosteroid signaling promotes reserve mobilization through the BZR1–RAmy3D module, sugar starvation is sensed through the SnRK1A-MYBS1 cascade, and under low oxygen the CIPK15–SnRK1A–MYBS1 pathway promotes α-amylase expression to sustain carbon supply during anaerobic germination. The OsNAC3 transcription factor directly activates the ABA catabolic gene OsABA8ox1 and the cell-expansion gene OsEXP4, and through an OsNAC3–OsITPK4–OsMT2b module limits excessive ROS accumulation, coordinating hormonal rebalancing, redox homeostasis, and embryo growth. Under stress, OsRAV1 contributes to germination and early seedling growth under salinity and has been evaluated after direct sowing into soil under controlled normal and saline conditions, though replicated field validation remains absent; OsbHLH035 regulates ABA-dependent germination during salt exposure and ABA-independent growth recovery after stress removal; and the OsSAPK3–OsbZIP35 module defines osmotic-stress vigor through maintenance of redox balance during early germination. The review concludes that rice seed-vigor improvement should prioritize stage-appropriate regulatory alleles and precise modulation of transcription-factor activity—through promoter variants, phosphorylation sites, degrons, or partner interfaces—while jointly considering storability, dormancy and pre-harvest sprouting resistance, field establishment, yield, and grain quality, and that only regulators whose effects are reproducible under actual sowing conditions should be described as field-validated.

Subject of Research: Transcriptional regulation of rice seed vigor across seed development, storage, germination and seedling establishment, and its use in molecular breeding.

Article Title: Advances in the transcriptional regulation of seed vigor and its application in molecular breeding for rice

Article References: Chen, F., Zhang, Y., Wu, Z., Zhang, H., Gao, Y., Fan, J., Wei, Q., Xie, H., & Zhang, J. (2026). Advances in the transcriptional regulation of seed vigor and its application in molecular breeding for rice. Plant Molecular Biology, 116(6), Article 109. https://doi.org/10.1007/s11103-026-01772-0

Image Credits: AI Generated

DOI: 10.1007/s11103-026-01772-0

Keywords: rice, seed vigor, transcription factors, seed dormancy, pre-harvest sprouting, seed longevity, direct-seeded rice, ABA signaling, molecular breeding, genome editing, field emergence, multi-omics