GmYSL7 controls iron uptake, allocation, and cellular response of nodules in soybean.

Iron (Fe) is essential for DNA synthesis, photosynthesis and respiration of plants. The demand for Fe substantially increases during legumes-rhizobia symbiotic nitrogen fixation because of the synthesis of leghemoglobin in the host and Fe-containing proteins in bacteroids. However, the mechanism by which plant controls iron transport to nodules remains largely unknown. Here we demonstrate that GmYSL7 serves as a key regulator controlling Fe uptake from root to nodule and distribution in soybean nodules. GmYSL7 is Fe responsive and GmYSL7 transports iron across the membrane and into the infected cells of nodules. Alterations of GmYSL7 substantially affect iron distribution between root and nodule, resulting in defective growth of nodules and reduced nitrogenase activity. GmYSL7 knockout increases the expression of GmbHLH300, a transcription factor required for Fe response of nodules. Overexpression of GmbHLH300 decreases nodule number, nitrogenase activity and Fe content in nodules. Remarkably, GmbHLH300 directly binds to the promoters of ENOD93 and GmLbs, which regulate nodule number and nitrogenase activity, and represses their transcription. Our data reveal a new role of GmYSL7 in controlling Fe transport from host root to nodule and Fe distribution in nodule cells, and uncover a molecular mechanism by which Fe affects nodule number and nitrogenase activity.

The B-type response regulator GmRR11d mediates systemic inhibition of symbiotic nodulation.

Key to the success of legumes is the ability to form and maintain optimal symbiotic nodules that enable them to balance the trade-off between symbiosis and plant growth. Cytokinin is essential for homeostatic regulation of nodulation, but the mechanism remains incompletely understood. Here, we show that a B-type response regulator GmRR11d mediates systemic inhibition of nodulation. GmRR11d is induced by rhizobia and low level cytokinin, and GmRR11d can suppress the transcriptional activity of GmNSP1 on GmNIN1a to inhibit soybean nodulation. GmRR11d positively regulates cytokinin response and its binding on the GmNIN1a promoter is enhanced by cytokinin. Intriguingly, rhizobial induction of GmRR11d and its function are dependent upon GmNARK that is a CLV1-like receptor kinase and inhibits nodule number in shoots. Thus, GmRR11d governs a transcriptional program associated with nodulation attenuation and cytokinin response activation essential for systemic regulation of nodulation.

NUCLEAR PORE ANCHOR and EARLY IN SHORT DAYS 4 negatively regulate abscisic acid signaling by inhibiting Snf1-related protein kinase2 activity and stability in Arabidopsis.

Abscisic acid (ABA) is a key regulator of plant responses to abiotic stresses, such as drought. Abscisic acid receptors and coreceptors perceive ABA to activate Snf1-related protein kinase2s (SnRK2s) that phosphorylate downstream effectors, thereby activating ABA signaling and the stress response. As stress responses come with fitness penalties for plants, it is crucial to tightly control SnRK2 kinase activity to restrict ABA signaling. However, how SnRK2 kinases are inactivated remains elusive. Here, we show that NUCLEAR PORE ANCHOR (NUA), a nuclear pore complex (NPC) component, negatively regulates ABA-mediated inhibition of seed germination and post-germination growth, and drought tolerance in Arabidopsis thaliana. The role of NUA in response to ABA depends on SnRK2.2 and SnRK2.3 for seed germination and on SnRK2.6 for drought. NUA does not directly inhibit the phosphorylation of these SnRK2s or affects their abundance. However, the NUA-interacting protein EARLY IN SHORT DAYS 4 (ESD4), a SUMO protease, negatively regulates ABA signaling by directly interacting with and inhibiting SnRK2 phosphorylation and protein levels. More importantly, we demonstrated that SnRK2.6 can be SUMOylated in vitro, and ESD4 inhibits its SUMOylation. Taken together, we identified NUA and ESD4 as SnRK2 kinase inhibitors that block SnRK2 activity, and reveal a mechanism whereby NUA and ESD4 negatively regulate plant responses to ABA and drought stress possibly through SUMOylation-dependent regulation of SnRK2s.

GmbZIP1 negatively regulates ABA-induced inhibition of nodulation by targeting GmENOD40-1 in soybean.

BACKGROUND: Abscisic acid (ABA) plays an important role in plant growth and adaptation through the ABA signaling pathway. The ABA-responsive element binding (AREB/ABF) family transcriptional factors are central regulators that integrate ABA signaling with various signaling pathways. It has long been known that ABA inhibits rhizobial infection and nodule formation in legumes, but the underlying molecular mechanisms remain elusive. RESULTS: Here, we show that nodulation is very sensitive to ABA and exogenous ABA dramatically inhibits rhizobial infection and nodule formation in soybean. In addition, we proved that GmbZIP1, an AREB/ABF transcription factor, is a major regulator in both nodulation and plant response to ABA in soybean. GmbZIP1 was specifically expressed during nodule formation and development. Overexpression of GmbZIP1 resulted in reduced rhizobial infection and decreased nodule number. Furthermore, GmbZIP1 is responsive to ABA, and ectopic overexpression of GmbZIP1 increased sensitivity of Arabidopsis plants to ABA during seed germination and postgerminative growth, and conferred enhanced drought tolerance of plants. Remarkably, we found that GmbZIP1 directly binds to the promoter of GmENOD40-1, a marker gene for nodule formation, to repress its expression. CONCLUSION: Our results identified GmbZIP1 as a node regulator that integrates ABA signaling with nodulation signaling to negatively regulate nodule formation.

Counteraction of ABA-Mediated Inhibition of Seed Germination and Seedling Establishment by ABA Signaling Terminator in Arabidopsis.

Seed germination and seedling establishment are important for the reproductive success of plants, but seeds and seedlings typically encounter constantly changing environmental conditions. By inhibiting seed germination and post-germinative growth through the PYR1/PYL/RCAR ABA receptors and PP2C co-receptors, the phytohormone abscisic acid (ABA) prevents premature germination and seedling growth under unfavorable conditions. However, little is known about how the ABA-mediated inhibition of seed germination and seedling establishment is thwarted. Here, we report that ABA Signaling Terminator (ABT), a WD40 protein, efficiently switches off ABA signaling and is critical for seed germination and seedling establishment. ABT is induced by ABA in a PYR1/PYL/RCAR-PP2C-dependent manner. Overexpression of ABT promotes seed germination and seedling greening in the presence of ABA, whereas knockout of ABT has the opposite effect. We found that ABT interacts with the PYR1/PYL/RCAR and PP2C proteins, interferes with the interaction between PYR1/PYL4 and ABI1/ABI2, and hampers the inhibition of ABI1/ABI2 by ABA-bound PYR1/PYL4, thereby terminating ABA signaling. Taken together, our results reveal a core mechanism of ABA signaling termination that is critical for seed germination and seedling establishment in Arabidopsis.

GAI Functions in the Plant Response to Dehydration Stress in Arabidopsis thaliana.

DELLA (GAI/RGA/RGL1/RGL2/RGL3) proteins are key negative regulators in GA (gibberellin) signaling and are involved in regulating plant growth as a response to environmental stresses. It has been shown that the DELLA protein PROCERA (PRO) in tomato promotes drought tolerance, but its molecular mechanism remains unknown. Here, we showed that the gai-1 (gibberellin insensitive 1) mutant (generated from the gai-1 (Ler) allele (with a 17 amino acid deletion within the DELLA domain of GAI) by backcrossing gai-1 (Ler) with Col-0 three times), the gain-of-function mutant of GAI (GA INSENSITIVE) in Arabidopsis, increases drought tolerance. The stomatal density of the gai-1 mutant was increased but its stomatal aperture was decreased under abscisic acid (ABA) treatment conditions, suggesting that the drought tolerance of the gai-1 mutant is a complex trait. We further tested the interactions between DELLA proteins and ABF2 (abscisic acid (ABA)-responsive element (ABRE)-binding transcription factors) and found that there was a strong interaction between DELLA proteins and ABF2. Our results provide new insight into DELLA proteins and their role in drought stress tolerance.

Author Correction: Deep-sea Sediment Resuspension by Internal Solitary Waves in the Northern South China Sea.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Deep-sea Sediment Resuspension by Internal Solitary Waves in the Northern South China Sea.

Internal solitary waves (ISWs) can cause strong vertical and horizontal currents and turbulent mixing in the ocean. These processes affect sediment and pollutant transport, acoustic transmissions and man-made structures in the shallow and deep oceans. Previous studies of the role of ISWs in suspending seafloor sediments and forming marine nepheloid layers were mainly conducted in shallow-water environments. In summer 2017, we observed at least four thick (70-140 m) benthic nepheloid layers (BNLs) at water depths between 956 and 1545 m over continental slopes in the northern South China Sea. We found there was a good correlation between the timing of the ISW packet and variations of the deepwater suspended sediment concentration (SSC). At a depth of 956 m, when the ISW arrived, the near-bottom SSC rapidly increased by two orders of magnitude to 0.62 mg/l at 8 m above the bottom. At two much deeper stations, the ISW-induced horizontal velocity reached 59.6-79.3 cm/s, which was one order of magnitude more than the seafloor contour currents velocity. The SSC, 10 m above the sea floor, rapidly increased to 0.10 mg/l (depth of 1545 m) and 1.25 mg/l (depth of 1252 m). In this study, we found that ISWs could suspend much more sediments on deepwater areas than previously thought. Specifically, we estimated that ISWs could induce and suspend 78.7 Mt/yr of sediment from shelf to deep-sea areas of the northern South China Sea. The total amount of sediment resuspended by shoaling ISWs was 2.7 times that of river-derived sediment reaching the northern South China Sea. This accounted for 6.1% of the global river-discharged sediment (16.4% of that from Asian rivers) transported to the sea.

SCFAtPP2-B11 modulates ABA signaling by facilitating SnRK2.3 degradation in Arabidopsis thaliana.

The phytohormone abscisic acid (ABA) is an essential part of the plant response to abiotic stressors such as drought. Upon the perception of ABA, pyrabactin resistance (PYR)/PYR1-like (PYL)/regulatory components of ABA receptor (RCAR) proteins interact with co-receptor protein phosphatase type 2Cs to permit activation Snf1-related protein kinase2 (SnRK2) kinases, which switch on ABA signaling by phosphorylating various target proteins. Thus, SnRK2 kinases are central regulators of ABA signaling. However, the mechanisms that regulate SnRK2 degradation remain elusive. Here, we show that SnRK2.3 is degradated by 26S proteasome system and ABA promotes its degradation. We found that SnRK2.3 interacts with AtPP2-B11 directly. AtPP2-B11 is an F-box protein that is part of a SKP1/Cullin/F-box E3 ubiquitin ligase complex that negatively regulates plant responses to ABA by specifically promoting the degradation of SnRK2.3. AtPP2-B11 was induced by ABA, and the knockdown of AtPP2-B11 expression markedly increased the ABA sensitivity of plants during seed germination and postgerminative development. Overexpression of AtPP2-B11 does not affect ABA sensitivity, but inhibits the ABA hypersensitive phenotypes of SnRK2.3 overexpression lines. These results reveal a novel mechanism through which AtPP2-B11 specifically degrades SnRK2.3 to attenuate ABA signaling and the abiotic stress response in Arabidopsis.