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Transcriptome Analysis Unravels Key Factors Involved in Response to Potassium Deficiency and Feedback Regulation of K+ Uptake in Cotton Roots

ABSTRACT: To properly understand cotton responses to potassium (K+) deficiency and how its shoot feedback regulates K+ uptake and root growth, we analyzed the changes in root transcriptome induced by low K+ (0.03 mM K+, lasting three days) in self-grafts of a K+ inefficient cotton variety (CCRI41/CCRI41, scion/rootstock) and its reciprocal grafts with a K+ efficient variety (SCRC22/CCRI41). Compared with CCRI41/CCRI41, the SCRC22 scion enhanced the K+ uptake and root growth of CCRI41 rootstock. A total of 1968 and 2539 differently expressed genes (DEGs) were identified in the roots of CCRI41/CCRI41 and SCRC22/CCRI41 in response to K+ deficiency, respectively. The overlapped and similarly (both up- or both down-) regulated DEGs in the two grafts were considered the basic response to K+ deficiency in cotton roots, whereas the DEGs only found in SCRC22/CCRI41 (1954) and those oppositely (one up- and the other down-) regulated in the two grafts might be the key factors involved in the feedback regulation of K+ uptake and root growth. The expression level of four putative K+ transporter genes (three GhHAK5s and one GhKUP3) increased in both grafts under low K+, which could enable plants to cope with K+ deficiency. In addition, two ethylene response factors (ERFs), GhERF15 and GhESE3, both down-regulated in the roots of CCRI41/CCRI41 and SCRC22/CCRI41, may negatively regulate K+ uptake in cotton roots due to higher net K+ uptake rate in their virus-induced gene silencing (VIGS) plants. In terms of feedback regulation of K+ uptake and root growth, several up-regulated DEGs related to Ca2+ binding and CIPK (CBL-interacting protein kinases), one up-regulated GhKUP3 and several up-regulated GhNRT2.1s probably play important roles. In conclusion, these results provide a deeper insight into the molecular mechanisms involved in basic response to low K+ stress in cotton roots and feedback regulation of K+ uptake, and present several low K+ tolerance-associated genes that need to be further identified and characterized.

SUBMITTER: Yang D

PROVIDER: S-EPMC8003395 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Cadmium (Cd), a non-essential element for plant, is a ubiquitous and highly toxic heavy metal, seriously endangering agricultural production and human health. As a nonedible economic crop, cotton (Gossypium hirsutum L.) has great potential in remediation of Cd contaminated soil, but its underlying mechanism is still unknown. Melatonin (MT), as a plant growth regulator, is involved in alleviating Cd toxicity in some plants, but the molecular mechanisms of MT-mediated Cd detoxification in cotton are largely unknown. This study investigated the possible molecular mechanisms of the MT-mediated Cd detoxification in cotton seedlings by comparative transcriptomic and metabolomic analyses. The results showed that the cotton seedlings were dwarfed and the leaves were wilted and yellow under Cd stress. The application of 50 µmol L−1 MT significantly increased the superoxide dismutase (SOD) activity and malondialdehyde (MDA) content under Cd stress, but 100 µmol L−1 MT significantly decreased SOD activity, while increased ascorbate peroxidase (APX) activity significantly. The addition of 100 μmol L−1 MT significantly increased Cd concentration in the shoots and roots under Cd stress. RNA-seq analysis showed that 5573, 7105, 7253, 25, 198, 9 up-regulated and 6644, 7192, 7404, 9, 59, 0 down-regulated differentially expressed genes (DEGs) were identified in the comparisons of CK vs T1, CK vs T2, CK vs T3, T1 vs T2, T1 vs T3 and T2 vs T3, respectively. It was revealed that MT promoted the expression of certain related genes under Cd stress, and the effect of 100 µmol L−1 MT was better. Moreover, UPLC-MS/MS widely targeted metabolites analyses showed that 195, 150, 150, 12, 24, 59 up-regulated and 16, 11, 23, 38, 127, 66 down-regulated differentially accumulated metabolites (DAMs) were changed in the CK vs T1, CK vs T2, CK vs T3, T1 vs T2, T1 vs T3 and T2 vs T3, respectively. It was revealed that MT induced the synthesis of alkaloids and flavonoids, and inhibited or reduced the synthesis of lipids, amino acids and their derivatives. The comprehensive analyses of transcriptomic and metabolic data showed that 33 DEGs and 4 DAMs, 46 DEGs and 16 DAMs, and 1 DEGs and 1 DAMs were dominantly involved in the pathways of valine, leucine and isoleucine degradation, ABC transporter, alpha-linolenic acid metabolism, respectively. It was revealed that there were three major mechanisms involved in MT-mediated Cd detoxification in cotton, including the enhancement of antioxidant capacity regulated by APX, flavonoids and alkaloids; accumulation of secondary metabolites related to Cd chelation, such as amino acids and derivatives; and regulation of cadmium ion transportation, such as ABC transporter activation. In conclusion, this study provides new insights into the MT-mediated Cd stress response.

Project description:BackgroundPotassium (K+) is an important nutrient ion in plant cells and plays crucial roles in many plant physiological and developmental processes. In the natural environment, K+ deficiency is a common abiotic stress that inhibits plant growth and reduces crop productivity. Several microarray studies have been conducted on genome-wide gene expression profiles of rice during its responses to various stresses. However, little is known about the transcriptional changes in rice genes under low-K+ conditions.ResultsWe analyzed the transcriptomic profiles of rice roots in response to low-K+ stress. The roots of rice seedlings with or without low-K+ treatment were harvested after 6 h, and 3 and 5 d, and used for microarray analysis. The microarray data showed that many genes (2,896) were up-regulated or down-regulated more than 1.2-fold during low-K+ treatment. GO analysis indicated that the genes showing transcriptional changes were mainly in the following categories: metabolic process, membrane, cation binding, kinase activity, transport, and so on. We conducted a comparative analysis of transcriptomic changes between Arabidopsis and rice under low-K+ stress. Generally, the genes showing changes in transcription in rice and Arabidopsis in response to low-K+ stress displayed similar GO distribution patterns. However, there were more genes related to stress responses and development in Arabidopsis than in rice. Many auxin-related genes responded to K+ deficiency in rice, whereas jasmonic acid-related enzymes may play more important roles in K+ nutrient signaling in Arabidopsis.ConclusionsAccording to the microarray data, fewer rice genes showed transcriptional changes in response to K+ deficiency than to phosphorus (P) or nitrogen (N) deficiency. Thus, transcriptional regulation is probably more important in responses to low-P and -N stress than to low-K+ stress. However, many genes in some categories (protein kinase and ion transporter families) were markedly up-regulated, suggesting that they play important roles during K+ deficiency. Comparative analysis of transcriptomic changes between Arabidopsis and rice showed that monocots and dicots share many similar mechanisms in response to K+ deficiency, despite some differences. Further research is required to clarify the differences in transcriptional regulation between monocots and dicots.

Project description:BackgroundAs one of three essential nutrients, potassium is regarded as a main limiting factor for growth and development in plant. Sweet potato (Ipomoea batatas L.) is one of seven major food crops grown worldwide, and is both a nutrient-rich food and a bioenergy crop. It is a typical 'K-favoring' crop, and the level of potassium ion (K+) supplementation directly influences its production. However, little is known about the transcriptional changes in sweet potato genes under low-K+ conditions. Here, we analyzed the transcriptomic profiles of sweet potato roots in response to K+ deficiency to determine the effect of low-K+ stress on this economically important crop.ResultsThe roots of sweet potato seedlings with or without K+ treatment were harvested and used for transcriptome analyses. The results showed 559 differently expressed genes (DEGs) in low and high K+ groups. Among the DEGs, 336 were upregulated and 223 were downregulated. These DEGs were involved in transcriptional regulation, calcium binding, redox-signaling, biosynthesis, transport, and metabolic process. Further analysis revealed previously unknow genes involved in low-K+ stress, which could be investigated further to improve low K+ tolerance in plants. Confirmation of RNA-sequencing results using qRT-PCR displayed a high level of consistency between the two experiments. Analysis showed that many auxin-, ethylene- and jasmonic acid-related genes respond to K+ deficiency, suggesting that these hormones have important roles in K+ nutrient signaling in sweet potato.ConclusionsAccording to the transcriptome data of sweet potato, various DEGs showed transcriptional changes in response to low-K+ stress. However, the expression level of some kinases, transporters, transcription factors (TFs), hormone-related genes, and plant defense-related genes changed significantly, suggesting that they have important roles during K+ deficiency. Thus, this study identifies potential genes for genetic improvement of responses to low-K+ stress and provides valuable insight into the molecular mechanisms regulating low K+ tolerance in sweet potato. Further research is required to clarify the function of these DEGs under low-K+ stress.

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Transcriptome Analysis Unravels Key Factors Involved in Response to Potassium Deficiency and Feedback Regulation of K+ Uptake in Cotton Roots

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