Genome accessibility dynamics in response to phosphate limitation is controlled by the PHR1 family of transcription factors in Arabidopsis.

As phosphorus is one of the most limiting nutrients in many natural and agricultural ecosystems, plants have evolved strategies that cope with its scarcity. Genetic approaches have facilitated the identification of several molecular elements that regulate the phosphate (Pi) starvation response (PSR) of plants, including the master regulator of the transcriptional response to phosphate starvation PHOSPHATE STARVATION RESPONSE1 (PHR1). However, the chromatin modifications underlying the plant transcriptional response to phosphate scarcity remain largely unknown. Here, we present a detailed analysis of changes in chromatin accessibility during phosphate starvation in Arabidopsis thaliana root cells. Root cells undergo a genome-wide remodeling of chromatin accessibility in response to Pi starvation that is often associated with changes in the transcription of neighboring genes. Analysis of chromatin accessibility in the phr1 phl2 double mutant revealed that the transcription factors PHR1 and PHL2 play a key role in remodeling chromatin accessibility in response to Pi limitation. We also discovered that PHR1 and PHL2 play an important role in determining chromatin accessibility and the associated transcription of many genes under optimal Pi conditions, including genes involved in the PSR. We propose that a set of transcription factors directly activated by PHR1 in Pi-starved root cells trigger a second wave of epigenetic changes required for the transcriptional activation of the complete set of low-Pi-responsive genes.

Prospects of genetics and breeding for low-phosphate tolerance: an integrated approach from soil to cell.

Improving phosphorus (P) crop nutrition has emerged as a key factor toward achieving a more resilient and sustainable agriculture. P is an essential nutrient for plant development and reproduction, and phosphate (Pi)-based fertilizers represent one of the pillars that sustain food production systems. To meet the global food demand, the challenge for modern agriculture is to increase food production and improve food quality in a sustainable way by significantly optimizing Pi fertilizer use efficiency. The development of genetically improved crops with higher Pi uptake and Pi-use efficiency and higher adaptability to environments with low-Pi availability will play a crucial role toward this end. In this review, we summarize the current understanding of Pi nutrition and the regulation of Pi-starvation responses in plants, and provide new perspectives on how to harness the ample repertoire of genetic mechanisms behind these adaptive responses for crop improvement. We discuss on the potential of implementing more integrative, versatile, and effective strategies by incorporating systems biology approaches and tools such as genome editing and synthetic biology. These strategies will be invaluable for producing high-yielding crops that require reduced Pi fertilizer inputs and to develop a more sustainable global agriculture.

MEDIATOR16 orchestrates local and systemic responses to phosphate scarcity in Arabidopsis roots.

Phosphate (Pi ) is a critical macronutrient for the biochemical and molecular functions of cells. Under phosphate limitation, plants manifest adaptative strategies to increase phosphate scavenging. However, how low phosphate sensing links to the transcriptional machinery remains unknown. The role of the MEDIATOR (MED) transcriptional co-activator, through its MED16 subunit in Arabidopsis root system architecture remodeling in response to phosphate limitation was assessed. Its critical function acting over the SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1)-ALUMINUM-ACTIVATED MALATE TRANSPORT1 (ALMT1) signaling module was tested through a combination of genetic, biochemical, and genome-wide transcriptomic approaches. Root system configuration in response to phosphate scarcity involved MED16 functioning, which modulates the expression of a large set of low-phosphate-induced genes that respond to local and systemic signals in the Arabidopsis root tip, including those directly activated by STOP1. Biomolecular fluorescence complementation analysis suggests that MED16 is required for the transcriptional activation of STOP1 targets, including the membrane permease ALMT1, to increase malate exudation in response to low phosphate. Our results unveil the function of a critical transcriptional component, MED16, in the root adaptive responses to a scarce plant macronutrient, which helps understanding how plant cells orchestrate root morphogenesis to gene expression with the STOP1-ALMT1 module.

Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate.

Low phosphate (Pi) availability constrains plant development and seed production in both natural and agricultural ecosystems. When Pi is scarce, modifications of root system architecture (RSA) enhance the soil exploration ability of the plant and lead to an increase in Pi uptake. In Arabidopsis, an iron-dependent mechanism reprograms primary root growth in response to low Pi availability. This program is activated upon contact of the root tip with low-Pi media and induces premature cell differentiation and the arrest of mitotic activity in the root apical meristem, resulting in a short-root phenotype. However, the mechanisms that regulate the primary root response to Pi-limiting conditions remain largely unknown. Here we report on the isolation and characterization of two low-Pi insensitive mutants (lpi5 and lpi6), which have a long-root phenotype when grown in low-Pi media. Cellular, genomic, and transcriptomic analysis of low-Pi insensitive mutants revealed that the genes previously shown to underlie Arabidopsis Al tolerance via root malate exudation, known as SENSITIVE TO PROTON RHIZOTOXICITY (STOP1) and ALUMINUM ACTIVATED MALATE TRANSPORTER 1 (ALMT1), represent a critical checkpoint in the root developmental response to Pi starvation in Arabidopsis thaliana Our results also show that exogenous malate can rescue the long-root phenotype of lpi5 and lpi6 Malate exudation is required for the accumulation of Fe in the apoplast of meristematic cells, triggering the differentiation of meristematic cells in response to Pi deprivation.

Beneficial Effects of Phosphite in Arabidopsis thaliana Mediated by Activation of ABA, SA, and JA Biosynthesis and Signaling Pathways.

Phosphite (Phi) has gained attention in agriculture due to its biostimulant effect on crops. This molecule has been found to benefit plant performance by providing protection against pathogens, improving yield and fruit quality as well as nutrient and water use efficiency. It is still unclear how Phi enhances plant growth and protects against multiple stresses. It has been hypothesized that Phi acts by directly affecting the pathogens and interacting with the plant cellular components and molecular machinery to elicit defense responses. This study elucidates the mechanisms underlying Phi's beneficial effects on plants, revealing their complex interplay with fundamental signaling pathways. An RNA-seq study of Arabidopsis seedlings under optimal and limiting phosphate conditions helped us unveil Phi's role in promoting plant growth by activating the expression of the genes involved in the biosynthesis and signaling pathways associated with abscisic acid (ABA), salicylic acid (SA), and jasmonic acid (JA). The expression of ABA-related genes, known for their involvement in stress response and development regulation, is triggered by Phi treatment, contributing to enhanced resilience and growth. Simultaneously, the activation of the SA pathway, associated with defense responses, suggests Phi's potential in bolstering plant immunity. Moreover, Phi influences JA biosynthesis and signaling, which are crucial for defense against herbivores and pathogens, thereby strengthening plants' defenses. Our findings reveal a multifaceted mechanism through which Phi benefits Arabidopsis development. Understanding its intricate interplay with key signaling pathways opens avenues for leveraging Phi as a strategic tool to enhance plant resilience, immunity, and growth in agricultural and ecological contexts.

Enhanced phenylpropanoid metabolism underlies resistance to Fusarium oxysporum f. sp. vasinfectum race 4 infection in the cotton cultivar Pima-S6 (Gossypium barbadense L.).

Introduction: Fusarium oxysporum f. sp. vasinfectum (FOV) race 4 (FOV4) is a highly pathogenic soil-borne fungus responsible for Fusarium wilt in cotton (Gossypium spp.) and represents a continuing threat to cotton production in the southwest states of the United States, including California, New Mexico, and Texas. Pima (G. barbadense L.) cotton, which is highly valued for its fiber quality, has been shown to be more susceptible to this pathogen than Upland (G. hirsutum L.) cotton. Still, some Pima cultivars present resistance to FOV4 infection. Methods: To gain insights into the FOV4-resistance mechanism, we performed comparative transcriptional and metabolomic analyses between FOV4-susceptible and FOV4-resistant Pima cotton entries. FOV4-resistant Pima-S6 and FOV4-susceptible Pima S-7 and Pima 3-79 cotton plants were infected with FOV4 in the greenhouse, and the roots harvested 11 days post-infection for further analysis. Results: We found that an enhanced root phenylpropanoid metabolism in the resistant Pima-S6 cultivar determines FOV4-resistance. Gene-ontology enrichment of phenylpropanoid biosynthesis and metabolism categories correlated with the accumulation of secondary metabolites in Pima-S6 roots. Specifically, we found esculetin, a coumarin, an inhibitor of Fusarium's growth, accumulated in the roots of Pima-S6 even under non-infected conditions. Genes related to the phenylpropanoid biosynthesis and metabolism, including phenylalanine ammonia-lyase 2 (PAL2) and pleiotropic drug resistance 12 (PDR12) transporter, were found to be upregulated in Pima-S6 roots. Discussion: Our results highlight an essential role for the phenylpropanoid synthesis pathway in FOV4 resistance in Pima-S6 cotton. These genes represent attractive research prospects for FOV4-disease resistance and breeding approaches of other cotton cultivars of economic relevance.

Root-Knot Nematode Resistance in Gossypium hirsutum Determined by a Constitutive Defense-Response Transcriptional Program Avoiding a Fitness Penalty.

Cotton (Gossypium spp.) is the most important renewable source of natural textile fiber and one of the most cultivated crops around the world. Plant-parasitic nematode infestations, such as the southern Root-Knot Nematode (RKN) Meloidogyne incognita, represent a threat to cotton production worldwide. Host-plant resistance is a highly effective strategy to manage RKN; however, the underlying molecular mechanisms of RKN-resistance remain largely unknown. In this study, we harness the differences in RKN-resistance between a susceptible (Acala SJ-2, SJ2), a moderately resistant (Upland Wild Mexico Jack Jones, WMJJ), and a resistant (Acala NemX) cotton entries, to perform genome-wide comparative analysis of the root transcriptional response to M. incognita infection. RNA-seq data suggest that RKN-resistance is determined by a constitutive state of defense transcriptional behavior that prevails in the roots of the NemX cultivar. Gene ontology and protein homology analyses indicate that the root transcriptional landscape in response to RKN-infection is enriched for responses related to jasmonic and salicylic acid, two key phytohormones in plant defense responses. These responses are constitutively activated in NemX and correlate with elevated levels of these two hormones while avoiding a fitness penalty. We show that the expression of cotton genes coding for disease resistance and receptor proteins linked to RKN-resistance and perception in plants, is enhanced in the roots of RKN-resistant NemX. Members of the later gene families, located in the confidence interval of a previously identified QTL associated with RKN resistance, represent promising candidates that might facilitate introduction of RKN-resistance into valuable commercial varieties of cotton. Our study provides novel insights into the molecular mechanisms that underlie RKN resistance in cotton.

Dissection of Root Transcriptional Responses to Low pH, Aluminum Toxicity and Iron Excess Under Pi-Limiting Conditions in Arabidopsis Wild-Type and stop1 Seedlings.

Acidic soils constrain plant growth and development in natural and agricultural ecosystems because of the combination of multiple stress factors including high levels of Fe3+, toxic levels of Al3+, low phosphate (Pi) availability and proton rhizotoxicity. The transcription factor SENSITIVE TO PROTON RHIZOTOXICITY (STOP1) has been reported to underlie root adaptation to low pH, Al3+ toxicity and low Pi availability by activating the expression of genes involved in organic acid exudation, regulation of pH homeostasis, Al3+ detoxification and root architecture remodeling in Arabidopsis thaliana. However, the mechanisms by which STOP1 integrates these environmental signals to trigger adaptive responses to variable conditions in acidic soils remain to be unraveled. It is unknown whether STOP1 activates the expression of a single set of genes that enables root adaptation to acidic soils or multiple gene sets depending on the combination of different types of stress present in acidic soils. Previous transcriptomic studies of stop1 mutants and wild-type plants analyzed the effect of individual types of stress prevalent in acidic soils. An integrative study of the transcriptional regulation pathways that are activated by STOP1 under the combination of major stresses common in acidic soils is lacking. Using RNA-seq, we performed a transcriptional dissection of wild-type and stop1 root responses, individually or in combination, to toxic levels of Al3+, low Pi availability, low pH and Fe excess. We show that the level of STOP1 is post-transcriptionally and coordinately upregulated in the roots of seedlings exposed to single or combined stress factors. The accumulation of STOP1 correlates with the transcriptional activation of stress-specific and common gene sets that are activated in the roots of wild-type seedlings but not in stop1. Our data indicate that perception of low Pi availability, low pH, Fe excess and Al toxicity converges at two levels via STOP1 signaling: post-translationally through the regulation of STOP1 turnover, and transcriptionally, via the activation of STOP1-dependent gene expression that enables the root to better adapt to abiotic stress factors present in acidic soils.

Adaptation to Phosphate Scarcity: Tips from Arabidopsis Roots.

Phosphorus (P) availability is a limiting factor for plant growth and development. Root tip contact with low Pi media triggers diverse changes in the root architecture of Arabidopsis thaliana. The most conspicuous among these modifications is the inhibition of root growth, which is triggered by a shift from an indeterminate to a determinate root growth program. This phenomenon takes place in the root tip and involves a reduction in cell elongation, a decrease in cell proliferation, and the induction of premature cell differentiation, resulting in meristem exhaustion. Here, we review recent findings in the root response of A. thaliana to low Pi availability and discuss the cellular and genetic basis of the inhibition of root growth in Pi-deprived seedlings.