Small particles, big effects: How nanoparticles can enhance plant growth in favorable and harsh conditions.

By 2050, the global population is projected to reach 9 billion, underscoring the imperative for innovative solutions to increase grain yield and enhance food security. Nanotechnology has emerged as a powerful tool, providing unique solutions to this challenge. Nanoparticles (NPs) can improve plant growth and nutrition under normal conditions through their high surface-to-volume ratio and unique physical and chemical properties. Moreover, they can be used to monitor crop health status and augment plant resilience against abiotic stresses (such as salinity, drought, heavy metals, and extreme temperatures) that endanger global agriculture. Application of NPs can enhance stress tolerance mechanisms in plants, minimizing potential yield losses and underscoring the potential of NPs to raise crop yield and quality. This review highlights the need for a comprehensive exploration of the environmental implications and safety of nanomaterials and provides valuable guidelines for researchers, policymakers, and agricultural practitioners. With thoughtful stewardship, nanotechnology holds immense promise in shaping environmentally sustainable agriculture amid escalating environmental challenges.

Incorporation of Selenium Derived from Nanoparticles into Plant Proteins in Vivo.

Diets comprising selenium-deficient crops have been linked to immune disorders and cardiomyopathy. Selenium nanoparticles (SeNPs) have emerged as a promising nanoplatform for selenium-biofortified agriculture. However, SeNPs fail to reach field-scale applications due to a poor understanding of the fundamental principles of its behavior. Here, we describe the transport, transformation, and bioavailability of SeNPs through a combination of in vivo and in vitro experiments. We show synthesized amorphous SeNPs, when sprayed onto the leaves of Arabidopsis thaliana, are rapidly biotransformed into selenium(IV), nonspecifically incorporated as selenomethionine (SeMet), and specifically incorporated into two selenium-binding proteins (SBPs). The SBPs identified were linked to stress and reactive oxygen species (mainly H2O2 and O2-) reduction, processes that enhance plant growth and primary root elongation. Selenium is transported both upwards and downwards in the plant when SeNPs are sprayed onto the leaves. With the application of Silwet L-77 (a common agrochemical surfactant), selenium distributed throughout the whole plant including the roots, where pristine SeNPs cannot reach. Our results demonstrate that foliar application of SeNPs promotes plant growth without causing nanomaterial accumulation, offering an efficient way to obtain selenium-fortified agriculture.

Magnetite nanoparticle coating chemistry regulates root uptake pathways and iron chlorosis in plants.

Understanding the fundamental interaction of nanoparticles at plant interfaces is critical for reaching field-scale applications of nanotechnology-enabled plant agriculture, as the processes between nanoparticles and root interfaces such as root compartments and root exudates remain largely unclear. Here, using iron deficiency-induced plant chlorosis as an indicator phenotype, we evaluated the iron transport capacity of Fe3O4 nanoparticles coated with citrate (CA) or polyacrylic acid (PAA) in the plant rhizosphere. Both nanoparticles can be used as a regulator of plant hormones to promote root elongation, but they regulate iron deficiency in plant in distinctive ways. In acidic root exudates secreted by iron-deficient Arabidopsis thaliana, CA-coated particles released fivefold more soluble iron by binding to acidic exudates mainly through hydrogen bonds and van der Waals forces and thus, prevented iron chlorosis more effectively than PAA-coated particles. We demonstrate through roots of mutants and visualization of pH changes that acidification of root exudates primarily originates from root tips and the synergistic mode of nanoparticle uptake and transformation in different root compartments. The nanoparticles entered the roots mainly through the epidermis but were not affected by lateral roots or root hairs. Our results show that magnetic nanoparticles can be a sustainable source of iron for preventing leaf chlorosis and that nanoparticle surface coating regulates this process in distinctive ways. This information also serves as an urgently needed theoretical basis for guiding the application of nanomaterials in agriculture.

NAC1 regulates root ground tissue maturation by coordinating with the SCR/SHR-CYCD6;1 module in Arabidopsis.

Precise spatiotemporal control of the timing and extent of asymmetric cell divisions (ACDs) is essential for plant development. In the Arabidopsis root, ground tissue maturation involves an additional ACD of the endodermis that maintains the inner cell layer as the endodermis and generates the middle cortex to the outside. Through regulation of the cell cycle regulator CYCLIND6;1 (CYCD6;1), the transcription factors SCARECROW (SCR) and SHORT-ROOT (SHR) play critical roles in this process. In the present study, we found that loss of function of NAC1, a NAC transcription factor family gene, causes markedly increased periclinal cell divisions in the root endodermis. Importantly, NAC1 directly represses the transcription of CYCD6;1 by recruiting the co-repressor TOPLESS (TPL), creating a fine-tuned mechanism to maintain proper root ground tissue patterning by limiting production of middle cortex cells. Biochemical and genetic analyses further showed that NAC1 physically interacts with SCR and SHR to restrict excessive periclinal cell divisions in the endodermis during root middle cortex formation. Although NAC1-TPL is recruited to the CYCD6;1 promoter and represses its transcription in an SCR-dependent manner, NAC1 and SHR antagonize each other to regulate the expression of CYCD6;1. Collectively, our study provides mechanistic insights into how the NAC1-TPL module integrates with the master transcriptional regulators SCR and SHR to control root ground tissue patterning by fine-tuning spatiotemporal expression of CYCD6;1 in Arabidopsis.

Correction: PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development in Arabidopsis thaliana.

[This corrects the article DOI: 10.1371/journal.pgen.1008044.].

How plants discern friends from foes.

Microbial-associated molecular pattern (MAMP)-triggered immunity (MTI) is a well-known plant innate immune response to pathogens. Plant commensal microbes have evolved a variety of strategies to interfere with or bypass MTI to establish symbiosis. Recent progress reported by Teixeira et al., Colaianni et al., Zhang et al., Fröschel et al., and Zhou et al. has been made in elucidating how commensal microbes regulate MTI.

Molecular Mechanism of Gibberellins in Mesocotyl Elongation Response to Deep-Sowing Stress in Sweet Maize.

Uneven germination is still a common problem in sweet maize planting. The mesocotyl is a key driver for ground-breaking sweet maize, and deep-sowing has a longer mesocotyl. However, the physiological and molecular mechanisms of sweet maize mesocotyl elongation in response to deep-sowing remain unknown. Here we found that sweet maize inbred line Ltx05 could obtain longer mesocotyls in deep soil of 10 cm depth, and that 20 mg/L GA3 was the optimal concentration to promote mesocotyl elongation and seedling emergence. Microstructure observation showed that the longitudinal cell length of mesocotyl at 10 cm sowing depth was significantly longer than that of 1 cm. Transcriptome analysis showed that microtubule process related differentially expressed genes may contribute to the longitudinal cell elongation. The content of GAs in the mesocotyl at 10 cm sowing depth was markedly higher than that of 1 cm. Combining transcriptome data and qRT-PCR at different developmental stages, ZmGA20ox1, ZmGA20ox4 and ZmGA20ox5 were identified as three positive regulation candidate genes during mesocotyl elongation under deep-sowing conditions, and this was further confirmed by the significant elongation of the hypocotyl in heterologous transformation of Arabidopsis thaliana. These results lay a foundation for improving the ability of sweet maize to tolerate deep-sowing stress and improving the breeding of excellent deep-sowing-tolerant germplasms.

The Arabidopsis Root Tip (Phospho)Proteomes at Growth-Promoting versus Growth-Repressing Conditions Reveal Novel Root Growth Regulators.

Auxin plays a dual role in growth regulation and, depending on the tissue and concentration of the hormone, it can either promote or inhibit division and expansion processes in plants. Recent studies have revealed that, beyond transcriptional reprogramming, alternative auxin-controlled mechanisms regulate root growth. Here, we explored the impact of different concentrations of the synthetic auxin NAA that establish growth-promoting and -repressing conditions on the root tip proteome and phosphoproteome, generating a unique resource. From the phosphoproteome data, we pinpointed (novel) growth regulators, such as the RALF34-THE1 module. Our results, together with previously published studies, suggest that auxin, H+-ATPases, cell wall modifications and cell wall sensing receptor-like kinases are tightly embedded in a pathway regulating cell elongation. Furthermore, our study assigned a novel role to MKK2 as a regulator of primary root growth and a (potential) regulator of auxin biosynthesis and signalling, and suggests the importance of the MKK2 Thr31 phosphorylation site for growth regulation in the Arabidopsis root tip.

Cell-type action specificity of auxin on Arabidopsis root growth.

The plant hormone auxin plays a critical role in root growth and development; however, the contributions or specific roles of cell-type auxin signals in root growth and development are not well understood. Here, we mapped tissue and cell types that are important for auxin-mediated root growth and development by manipulating the local response and synthesis of auxin. Repressing auxin signaling in the epidermis, cortex, endodermis, pericycle or stele strongly inhibited root growth, with the largest effect observed in the endodermis. Enhancing auxin signaling in the epidermis, cortex, endodermis, pericycle or stele also caused reduced root growth, albeit to a lesser extent. Moreover, we established that root growth was inhibited by enhancement of auxin synthesis in specific cell types of the epidermis, cortex and endodermis, whereas increased auxin synthesis in the pericycle and stele had only minor effects on root growth. Our study thus establishes an association between cellular identity and cell type-specific auxin signaling that guides root growth and development.

Light participates in the auxin-dependent regulation of plant growth.

Light is the energy source for plant photosynthesis and influences plant growth and development. Through multiple photoreceptors, plant interprets light signals through various downstream phytohormones such as auxin. Recently, Chen et al. (2020) uncover a new layer of regulation in IPyA pathway of auxin biosynthesis by light. Here we highlight recent studies about how light controls plant growth through regulating auxin biosynthesis and signaling.

Antagonistic Interaction between Auxin and SA Signaling Pathways Regulates Bacterial Infection through Lateral Root in Arabidopsis.

Pathogen entry into host tissues is a critical and first step in infections. In plants, the lateral roots (LRs) are a potential entry and colonization site for pathogens. Here, using a GFP-labeled pathogenic bacterium Pseudomonas syringae pv. tomato strain DC3000 (Pto DC3000), we observe that virulent Pto DC3000 invades plants through emerged LRs in Arabidopsis. Pto DC3000 strongly induced LR formation, a process that was dependent on the AUXIN RESPONSE FACTOR7 (ARF7)/ARF19-LATERAL ORGAN BOUNDARIES-DOMAIN (LBD) regulatory module. We show that salicylic acid (SA) represses LR formation, and several mutants defective in SA signaling are also involved in Pto DC3000-induced LR development. Significantly, ARF7, a well-documented positive regulator of LR development, directly represses the transcription of PR1 and PR2 to promote LR development. This study indicates that ARF7-mediated auxin signaling antagonizes with SA signaling to control bacterial infection through the regulation of LR development.

AtHB7/12 Regulate Root Growth in Response to Aluminum Stress.

Aluminum (Al) stress is a major limiting factor for plant growth and crop production in acid soils. At present, only a few transcription factors involved in the regulation of Al resistance have been characterized. Here, we used reversed genetic approach through phenotype analysis of overexpressors and mutants to demonstrate that AtHB7 and AtHB12, two HD-Zip I transcription factors, participate in Al resistance. In response to Al stress, AtHB7 and AtHB12 displayed different dynamic expression patterns. Although both AtHB7 and AtHB12 positively regulate root growth in the absence of Al stress, our results showed that AtHB7 antagonizes with AtHB12 to control root growth in response to Al stress. The athb7/12 double mutant displayed a wild-type phenotype under Al stress. Consistently, our physiological analysis showed that AtHB7 and AtHB12 oppositely regulate the capacity of cell wall to bind Al. Yeast two hybrid assays showed that AtHB7 and AtHB12 could form homo-dimers and hetero-dimers in vitro, suggesting the interaction between AtHB7 and AtHB12 in the regulation of root growth. The conclusion was that AtHB7 and AtHB12 oppositely regulate Al resistance by affecting Al accumulation in root cell wall.

PIFs coordinate shade avoidance by inhibiting auxin repressor ARF18 and metabolic regulator QQS.

Shade avoidance syndrome (SAS) arises in densely growing plants that compete for light. In Arabidopsis thaliana, phytochrome interacting factor (PIF) proteins link the perception of shade to stem elongation via auxin production. Here, we report that PIFs inhibit the shade-induced expression of AUXIN RESPONSE FACTOR 18 (ARF18), and ARF18 represses auxin signaling. Therefore, PIF-mediated inhibition of ARF18 enhances auxin-dependent hypocotyl elongation in simulated shade. Furthermore, we show that both PIFs and ARF18 directly repress qua-quine starch (QQS), which controls the allocation of carbon and nitrogen. Shade-repressed QQS attenuates the conversion of starch to protein and thus reduced leaf area. Our results suggest that PIF-dependent gene regulation coordinates multiple SAS responses, including altered stem growth via ARF18, as well as altered leaf growth and metabolism via QQS.

Differentially charged nanoplastics demonstrate distinct accumulation in Arabidopsis thaliana.

Although the fates of microplastics (0.1-5 mm in size) and nanoplastics (<100 nm) in marine environments are being increasingly well studied1,2, little is known about the behaviour of nanoplastics in terrestrial environments3-6, especially agricultural soils7. Previous studies have evaluated the consequences of nanoplastic accumulation in aquatic plants, but there is no direct evidence for the internalization of nanoplastics in terrestrial plants. Here, we show that both positively and negatively charged nanoplastics can accumulate in Arabidopsis thaliana. The aggregation promoted by the growth medium and root exudates limited the uptake of amino-modified polystyrene nanoplastics with positive surface charges. Thus, positively charged nanoplastics accumulated at relatively low levels in the root tips, but these nanoplastics induced a higher accumulation of reactive oxygen species and inhibited plant growth and seedling development more strongly than negatively charged sulfonic-acid-modified nanoplastics. By contrast, the negatively charged nanoplastics were observed frequently in the apoplast and xylem. Our findings provide direct evidence that nanoplastics can accumulate in plants, depending on their surface charge. Plant accumulation of nanoplastics can have both direct ecological effects and implications for agricultural sustainability and food safety.

Plant Sense: The Rise of Calcium Channels.

Although calcium (Ca2+) elevation triggered by abiotic and biotic stimuli has long been a documented phenomenon in plants, the mechanism underlying the control of Ca2+ spikes remains elusive. Recent progress, reported by Tian et al., Wang et al., Yu et al., Jiang et al., and Wu et al., has been made in elucidating how Ca2+ channels are controlled during pathogen attack, cell death, and salt or hydrogen peroxide sensing.

PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development in Arabidopsis thaliana.

The development of lateral roots in Arabidopsis thaliana is strongly dependent on signaling directed by the AUXIN RESPONSE FACTOR7 (ARF7), which in turn activates LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors (LBD16, LBD18 and LBD29). Here, the product of PRH1, a PR-1 homolog annotated previously as encoding a pathogen-responsive protein, was identified as a target of ARF7-mediated auxin signaling and also as participating in the development of lateral roots. PRH1 was shown to be strongly induced by auxin treatment, and plants lacking a functional copy of PRH1 formed fewer lateral roots. The transcription of PRH1 was controlled by the binding of both ARF7 and LBDs to its promoter region.

Initiation and maintenance of plant stem cells in root and shoot apical meristems.

Plant stem cells are a small group of cells with a self-renewal capacity and serve as a steady supply of precursor cells to form new differentiated tissues and organs in plants. Root stem cells and shoot stem cells, which are located in the root apical meristem and in the shoot apical meristem, respectively, play a critical role in plant longitudinal growth. These stem cells in shoot and root apical meristems remain as pluripotent state throughout the lifespan of the plant and control the growth and development of plants. The molecular mechanisms of initiation and maintenance of plant stem cells have been extensively investigated. In this review, we mainly discuss how the plant phytohormones, such as auxin and cytokinin, coordinate with the key transcription factors to regulate plant stem cell initiation and maintenance in root and shoot apical meristems. In addition, we highlight the common regulatory mechanisms of both root and shoot apical meristems.

Non-canonical AUX/IAA protein IAA33 competes with canonical AUX/IAA repressor IAA5 to negatively regulate auxin signaling.

The phytohormone auxin controls plant growth and development via TIR1-dependent protein degradation of canonical AUX/IAA proteins, which normally repress the activity of auxin response transcription factors (ARFs). IAA33 is a non-canonical AUX/IAA protein lacking a TIR1-binding domain, and its role in auxin signaling and plant development is not well understood. Here, we show that IAA33 maintains root distal stem cell identity and negatively regulates auxin signaling by interacting with ARF10 and ARF16. IAA33 competes with the canonical AUX/IAA repressor IAA5 for binding to ARF10/16 to protect them from IAA5-mediated inhibition. In contrast to auxin-dependent degradation of canonical AUX/IAA proteins, auxin stabilizes IAA33 protein via MITOGEN-ACTIVATED PROTEIN KINASE 14 (MPK14) and does not affect IAA33 gene expression. Taken together, this study provides insight into the molecular functions of non-canonical AUX/IAA proteins in auxin signaling transduction.

RLCKs Bridge Plant Immune Receptors and MAPK Cascades.

Receptor-like cytoplasmic kinases (RLCKs) and MAP kinase (MAPK) cascades function downstream of diverse pattern recognition receptors (PRRs) to transduce immune signals. Recent studies identified two MAPK kinase kinases that are directly activated by RLCKs, and filled in a gap in immune signal transduction between PRR activation and the MAPK cascades.