Plant lncRNAs are enriched in and move systemically through the phloem in response to phosphate deficiency

Zhang, Zhaoliang; Zheng, Yi; Ham, Byung‐Kook; Zhang, Shupei; Fei, Zhangjun; Lucas, William J.

doi:10.1111/jipb.12715

Cited by 38 publications

(17 citation statements)

References 89 publications

(142 reference statements)

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“…Moreover, lncRNA not only governs the expression of the phosphate transporter gene Pho84 but also exerts linkage effects on prt lncRNA and pho1 genes in flanking regions [13]. Recent studies have shown that lncRNAs exert a non-cell-autonomous response to P deficiency and may act as systemic signaling agents at the whole-plant level to coordinate early P deficiency signals [14]. LncRNAs also play key roles in regulating mRNA levels of a large number of genes associated with P starvation responses [15].…”

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confidence: 99%

Transcriptome-wide identification of novel circular RNAs in soybean in response to low-phosphorus stress

Lü

et al. 2020

PLoS ONE

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Low-phosphorus (LP) stress is a major factor limiting the growth and yield of soybean. Circular RNAs (circRNAs) are novel noncoding RNAs that play a crucial role in plant responses to abiotic stress. However, how LP stress mediates the biogenesis of circRNAs in soybean remains unclear. Here, to explore the response mechanisms of circRNAs to LP stress, the roots of two representative soybean genotypes with different P-use efficiency, Bogao (a LPsensitive genotype) and Nannong 94156 (a LP-tolerant genotype), were used for the construction of RNA sequencing (RNA-seq) libraries and circRNA identification. In total, 371 novel circRNA candidates, including 120 significantly differentially expressed (DE) cir-cRNAs, were identified across different P levels and genotypes. More DE circRNAs were significantly regulated by LP stress in Bogao than in NN94156, suggesting that the tolerant genotype was less affected by LP stress than the sensitive genotype was; in other words, NN94156 may have a better ability to maintain P homeostasis under LP stress. Moreover, a positive correlation was observed between the expression patterns of P stress-induced cir-cRNAs and their circRNA-host genes. Gene Ontology (GO) enrichment analysis of these circRNA-host genes and microRNA (miRNA)-targeted genes indicated that these DE cir-cRNAs were involved mainly in defense responses, ADP binding, nucleoside binding, organic substance catabolic processes, oxidoreductase activity, and signal transduction. Together, our results revealed that LP stress can significantly alter the genome-wide profiles of circRNAs and indicated that the regulation of circRNAs was both genotype and environment specific in response to LP stress. LP-induced circRNAs might provide a rich resource for LP-responsive circRNA candidates for future studies.

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confidence: 99%

Transcriptome-wide identification of novel circular RNAs in soybean in response to low-phosphorus stress

Lü

et al. 2020

PLoS ONE

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“…The absence of PHO2, an E2 ubiquitin-conjugating enzyme that represses phosphate uptake, allows for an increase in Pi loading into the xylem for transport to shoots (Figure 3, orange) [117,118,[176][177][178][179]. In addition, under phosphate limited conditions, many mRNA transcripts, including hormone receptors, TFs, and P i signaling genes like PHO2, as well as lncRNA transcripts like the target mimic of miRNA399 INDUCED BY PHOSPHATE STARVATION 1 (IPS1), are differentially expressed in source phloem and subsequently transported to sinks-developing leaves, the shoot apex, and root tips-in a tissue-specific manner [31,34,40]. While the exact mechanism and function of these mobile transcripts is still unknown, it is clear that a variety of RNA species are involved in the systemic early response to phosphate deficiency by coordinating nutrient perception between roots and shoots.…”

Section: Root Development and Nutrient Deficiencymentioning

confidence: 99%

“…Similarly, a cis -acting element within the 102 nucleotides at the 5′ end of FLOWERING LOCUS T (FT) is critical for the systemic transport of Arabidopsis FT RNA [ 37 ]. RNA-binding proteins play an important role in the translocation of some RNA species in the phloem; they contain motifs, like CU-rich polypyrimidine-binding regions, which can facilitate RNA binding and transport [ 34 , 35 , 38 ]. Additionally, other sequence motifs and secondary structures, such as tRNA-like structures, may also promote transcript mobility in the phloem [ 39 ].…”

Section: Introductionmentioning

confidence: 99%

The interplay of phloem-mobile signals in plant development and stress response

Koenig

Hoffmann-Benning

2020

Bioscience Reports

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Plants integrate a variety of biotic and abiotic factors for optimal growth in their given environment. While some of these responses are local, others occur distally. Hence, communication of signals perceived in one organ to a second, distal part of the plant and the coordinated developmental response require an intricate signaling system. To do so, plants developed a bipartite vascular system that mediates the uptake of water, minerals, and nutrients from the soil; transports high-energy compounds and building blocks; and traffics essential developmental and stress signals. One component of the plant vasculature is the phloem. The development of highly sensitive mass spectrometry and molecular methods in the last decades has enabled us to explore the full complexity of the phloem content. As a result, our view of the phloem has evolved from a simple transport path of photoassimilates to a major highway for pathogens, hormones, and developmental signals. Understanding phloem transport is essential to comprehend the coordination of environmental inputs with plant development and, thus, ensure food security. This review discusses recent developments in its role in long-distance signaling and highlights the role of some of the signaling molecules. What emerges is an image of signaling paths that do not involve single molecules but rather, quite frequently an interplay of several distinct molecular classes, many of which appear to be transported and acting in concert.

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“…The best example of this is plant response to P deficiency, which triggers massive changes in the phloem transcriptome and proteome (Zhang et al, 2016;Zhang Z. et al, 2019). The first example of P deficiency systemic signaling involves the microRNA 399 (mirR399), which is induced early in the low-P response in leaves and moves to the root in the phloem to interact with its target, the PHO2 gene (Fujii et al, 2005;Chiou et al, 2006;Hu et al, 2015).…”

Section: P Deficiency Stress and Responsesmentioning

confidence: 99%

Root Adaptation via Common Genetic Factors Conditioning Tolerance to Multiple Stresses for Crops Cultivated on Acidic Tropical Soils

et al. 2020

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Crop tolerance to multiple abiotic stresses has long been pursued as a Holy Grail in plant breeding efforts that target crop adaptation to tropical soils. On tropical, acidic soils, aluminum (Al) toxicity, low phosphorus (P) availability and drought stress are the major limitations to yield stability. Molecular breeding based on a small suite of pleiotropic genes, particularly those with moderate to major phenotypic effects, could help circumvent the need for complex breeding designs and large population sizes aimed at selecting transgressive progeny accumulating favorable alleles controlling polygenic traits. The underlying question is twofold: do common tolerance mechanisms to Al toxicity, P deficiency and drought exist? And if they do, will they be useful in a plant breeding program that targets stress-prone environments. The selective environments in tropical regions are such that multiple, co-existing regulatory networks may drive the fixation of either distinctly different or a smaller number of pleiotropic abiotic stress tolerance genes. Recent studies suggest that genes contributing to crop adaptation to acidic soils, such as the major Arabidopsis Al tolerance protein, AtALMT1, which encodes an aluminum-activated root malate transporter, may influence both Al tolerance and P acquisition via changes in root system morphology and architecture. However, trans -acting elements such as transcription factors (TFs) may be the best option for pleiotropic control of multiple abiotic stress genes, due to their small and often multiple binding sequences in the genome. One such example is the C2H2-type zinc finger, AtSTOP1, which is a transcriptional regulator of a number of Arabidopsis Al tolerance genes, including AtMATE and AtALMT1 , and has been shown to activate AtALMT1 , not only in response to Al but also low soil P. The large WRKY family of transcription factors are also known to affect a broad spectrum of phenotypes, some of which are related to acidic soil abiotic stress responses. Hence, we focus here on signaling proteins such as TFs and protein kinases to identify, from the literature, evidence for unifying regulatory networks controlling Al tolerance, P efficiency and, also possibly drought tolerance. Particular emphasis will be given to modification of root system morphology and architecture, which could be an important physiological “hub” leading to crop adaptation to multiple soil-based abiotic stress factors.

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Plant lncRNAs are enriched in and move systemically through the phloem in response to phosphate deficiency

Cited by 38 publications

References 89 publications

Transcriptome-wide identification of novel circular RNAs in soybean in response to low-phosphorus stress

Transcriptome-wide identification of novel circular RNAs in soybean in response to low-phosphorus stress

The interplay of phloem-mobile signals in plant development and stress response

Root Adaptation via Common Genetic Factors Conditioning Tolerance to Multiple Stresses for Crops Cultivated on Acidic Tropical Soils

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