2026/04/01 by Xiaoming Zheng, Qian Qian · 1 voice
Agricultural and Biological Sciences · #Legume Nitrogen Fixing Symbiosis #Plant nutrient uptake and metabolism #Rice Cultivation and Yield Improvement
paper · doi:10.1111/jipb.70247
openalex publication_date 2026/04/01 · openalex created_date 2026/04/02 · openalex updated_date 2026/07/28
The transcription factor WRINKLED1a coordinates nitrogen-responsive root and shoot growth in rice, improving nitrogen-use efficiency and yield stability. Under nitrogen (N) deficiency, plants typically allocate more biomass to roots in order to increase nutrient uptake capacity. This response arises from metabolic changes in the shoot and increased carbohydrate transport to roots, which leads to an increase in the root-to-shoot biomass ratio (Hermans et al., 2006). However, this reallocation often compromises shoot growth, which is disadvantageous for photosynthetic carbon gain and grain filling, ultimately constraining yield potential (Hermans et al., 2006; Wu et al., 2020). Rice (Oryza sativa L.), the staple food for more than half the global population, is central to world food security through stable and high grain yields. The Green Revolution of the 1960s, driven largely by widespread adoption of semi-dwarf cultivars carrying the sd1 allele, achieved substantial yield gains in rice (Sasaki et al., 2002). These varieties show reduced fertilizer responsiveness, increased lodging resistance, and improved harvest index, but often display low N-use efficiency (NUE) (Peng et al., 1999), necessitating heavy N fertilizer application to sustain yield increases. Excessive N inputs have caused widespread environmental damage, including soil acidification, water eutrophication, and elevated greenhouse gas emissions, as well as increased production costs (Ludemann et al., 2024). Thus, elucidating mechanisms that integrate NUE with whole-plant development and devising strategies for high yield under reduced N supply remain critical priorities for sustainable crop improvement and modern agriculture (Pingali, 2012). This work reframes NUE improvement as a coordination problem—not simply strengthening root foraging or shoot productivity alone, but stabilizing allocation plasticity through a tunable ubiquitination–transcription circuit. Li and colleagues recently reported a key advance in understanding integral N-responsive developmental regulation in rice (Shen et al., 2026). They identified OsWRI1a (WRINKLED1a) as a central regulatory hub that integrates N signaling to coordinate whole-plant growth, extending beyond its previously reported role in seed oil biosynthesis (Liu et al., 2022). Under N deficiency, OsWRI1a maintains dynamic root–shoot biomass by optimizing root system architecture to benefit nutrient-foraging capacity while supporting appropriate shoot growth. This bidirectional regulation enhances adaptation to low-N environments and overall resource-use efficiency. Notably, OsWRI1a stabilizes N-dependent root–shoot allocation without requiring altered carbon/sugar redistribution, suggesting an additional regulatory layer beyond the canonical shoot-to-root carbon flux. Prior work from the same group showed that low-N-induced root development in rice is tightly regulated by the RNR10–DNR1–auxin module. RNR10 is an F-box protein that targets DNR1, a negative regulator of auxin biosynthesis, for monoubiquitination at lysine 53 (K53). This modification stabilizes DNR1, increases its accumulation in roots, thereby suppressing auxin biosynthesis and modulating root development (Zhang et al., 2021; Huang et al., 2023). Their recent findings revealed that RNR10 also interacts with OsWRI1a and mediates its polyubiquitination at lysine residues K139, K156, and K225, which leads to its proteasomal degradation. OsWRI1a disrupts RNR10–DNR1 complex formation and reduces monoubiquitinated DNR1 levels, which indirectly promotes auxin accumulation to stimulate root growth. Moreover, as an AP2 transcription factor, OsWRI1a directly binds to the promoters of N metabolism genes, activating their expression to promote N uptake and assimilation, which at least partially contributes to root growth. Thus, OsWRI1a regulates root development through two complementary pathways by directly modulating nitrogen metabolism and fine-tuning local auxin homeostasis via the RNR10–DNR1 module, collectively optimizing root system architecture (Figure 1). Model of OsWRI1a-mediated coordination of N-dependent root–shoot allocation under low nitrogen and the contribution of the elite haplotype OsWRI1aHap.I (A) Schematic mechanism: Under low N, OsWRI1a acts as a central hub that directly activates genes involved in N uptake and assimilation, and optimizes root system architecture by modulating local auxin homeostasis through interference with the RNR10–DNR1 module. The SCF complex containing the F-box protein RNR10 functions as a substrate-selective ubiquitination switch, monoubiquitinating DNR1 to stabilize it while polyubiquitinating OsWRI1a to promote proteasomal degradation. In shoots, OsWRI1a directly upregulates the N-responsive regulator NGR5 to facilitate tiller outgrowth. (B, C) Phenotypic comparison: Under low N, the absence of OsWRI1aHap.I leads to a stronger shift of biomass allocation toward roots at the expense of shoot growth (B). In contrast, OsWRI1aHap.I stabilizes allocation plasticity across N regimes, maintaining shoot growth and yield potential while preserving root N acquisition capacity, thereby improving NUE (C). Tiller number increases with N abundance, primarily through the N-responsive transcription factor NGR5 (Wu et al., 2020). NGR5 recruits Polycomb Repressive Complex 2 (PRC2) to catalyze histone H3 lysine 27 trimethylation (H3K27me3) at tiller-inhibitory genes, thereby epigenetically repressing their expression and promoting tiller outgrowth. In the present study, OsWRI1a strongly upregulates NGR5 expression by direct promoter binding, thereby facilitating tiller bud outgrowth, enhancing photosynthetic efficiency, and promoting shoot development. Notably, OsWRI1a–RNR10 interaction is substantially weaker in tiller bud tissues than in roots (Figure 1). This tissue-specific reduction in binding attenuates RNR10-mediated polyubiquitination and degradation of OsWRI1a, preserving its activity in the shoot. To elucidate how RNR10 directs substrate-specific ubiquitination (monoubiquitination versus polyubiquitination), Shen et al. conducted biochemical and structural analyses. They show that differential recruitment of E2 ubiquitin-conjugating enzymes is necessary but not sufficient in determining the type of ubiquitination. An additional determining factor, the three-dimensional conformation of substrate–SKP1 complexes, also helps to determine the ubiquitination outcome in the SCFRNR10 complex. For DNR1, the monoubiquitination site K53 is buried in a narrow cleft near the RNR10–SKP1 interface, imposing steric hindrance that prevents ubiquitin chain elongation. In contrast, the polyubiquitination sites on OsWRI1a (K139, K156, and K225) are fully solvent-exposed, allowing unrestricted chain extension. These insights establish a mechanistic basis for substrate-selective ubiquitination by F-box proteins and highlight the multifunctional regulatory potential of SCF complexes. Furthermore, a superior allele, OsWRI1aHap.I, was identified with strong agronomic potential. This haplotype predominates in indica rice varieties and has been selectively enriched during breeding for N-limited environments. Geographic surveys confirmed its enrichment in varieties from southern China and other low-N paddy regions across Asia, consistent with signatures of ecological adaptation. Introgression of OsWRI1aHap.I into the japonica variety Wuyungeng 7 (WYJ7) enables the maintenance of a more stable root–shoot biomass ratio across N application levels than wild-type WYJ7 in multi-year, multi-site field trials. This stability supports robust root N acquisition without compromising shoot photosynthetic capacity. Consequently, the modified lines show substantially improved NUE and grain yield, delivering yield stability and significant fertilizer-saving benefits. In summary, this study presents novel findings on the synergistic regulation of N-responsive growth in both above- and below-ground tissues, and functionally validates OsWRI1a as a key regulator of NUE in rice production. Additionally, it broadens the genetic toolkit available for molecular breeding aimed at enhancing NUE. From an application perspective, the OsWRI1aHap.I allele emerges as a promising target for marker-assisted selection, genome editing, and precision breeding strategies. These approaches are expected to facilitate the development of high-yielding, low-input “green super rice” varieties, thereby contributing to the advancement of sustainable global agriculture. This work was supported by the Project of Sanya Yazhou Bay Science and Technology City (SKJC-JYRC-2023-47, SKJC-JYRC-2025-45), the Central Public-interest Scientific Institution Basal Research Fund (Y2025YC12) and the Innovational Fund for Scientific and Technological Personnel of Hainan Province (KJRC2023A01). The authors declare no conflicts of interest. Q.Q. conceptualized the idea. X.Z. wrote the draft. X.Z. and Q.Q. reviewed and revised the manuscript. All authors have read and approved the contents of this paper.