Identification of transcriptional regulators of the plant ionome

• Applicant: Dr. Ricardo F.H. Giehl
• Subject Area: Plant Physiology ; Plant Cultivation, Plant Nutrition, Agricultural Technology
• Term: from 2018 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 411711475

• Final Report Year: 2023

Final Report Abstract

The content of multiple elements in plant tissues (ionome) is a major determinant for plant growth and tolerance to a range of biotic and abiotic stresses. Besides being affected by the availability of mineral elements in the soil, several processes in plants including acquisition, uptake and long-distance transport, define the ionome of a plant throughout its development. Although transporters for most relevant inorganic ions have been identified and characterized, much less is known about the regulatory modules that regulate the accumulation of nutrients and trace elements in plants. Thus, the major goal of this project was to identify and characterize novel regulators of nutrient accumulation in Arabidopsis thaliana selected based on the shoot ionome of insertional mutants. Several mutants with altered accumulation of one or more element were identified. One of these mutants was itpk1, which exhibits two times higher phosphorus (P) concentration in shoots than wild-type plants. Characterization of ITPK1 revealed that this inositol polyphosphate kinase is critical for maintaining undisturbed P accumulation in plants. The ionomic phenotype was shown to result from ITPK1 role in P-dependent synthesis of the inositol pyrophosphates 5-InsP7 and InsP8, and to rely on the activity of the transcription factors PHR1 and PHL1. It was further demonstrated that under sufficient P supply and in the presence of high ATP levels, ITPK1 converts InsP6 to 5-InsP7 while under low ATP ITPK1 shift its activity and becomes an ADP phosphotransferase that dephosphorylates specifically 5-InsP7. Apart from ITPK1, the transcription factor NGATHA- LIKE 1 (NGAL1) was also found to regulate P accumulation in A. thaliana. Besides phosphorus, ngal1 mutants also accumulate higher concentrations of potassium (K). A transcriptome analysis revealed that many genes encoding for P and especially K transporters are deregulated in roots of the ngal1 mutant, suggesting that NGAL1 negatively regulates their expression. At the developmental level, NGAL1 affects root growth under low P but not low K. It was found that loss of NGAL1 results in increased iron (Fe) accumulation in the root apical meristem of plants grown on low P-containing medium, which coincides with ectopic callose deposition in columella cells and severe disorganization of the stem cell niche and quiescent center. Transcriptomics identified several genes related to Fe homeostasis and root stem cell niche maintenance deregulated in ngal1 roots, indicating that NGAL1 is a positive regulator of a mechanism that protects root meristems exposed to low external P concentrations. Finally, in the frame of the project, a method that combines fluorescence-activated cell sorting and ICP-MS was developed to determine the ionome of different cell populations of A. thaliana roots. The new method allows the quantification of multiple elements in different cell types and to explore the consequences of perturbed transport pathways or altered nutrient availabilities at high cell type resolution. Taken together, the results of this project revealed novel mechanisms regulating the plant ionome and developmental responses to nutrient availabilities.

Publications

• Arabidopsis inositol polyphosphate kinases IPK1 and ITPK1 modulate crosstalk between SA-dependent immunity and phosphate-starvation responses. Plant Cell Reports, 41(2), 347-363.
  Gulabani, Hitika; Goswami, Krishnendu; Walia, Yashika; Roy, Abhisha; Noor, Jewel Jameeta; Ingole, Kishor D.; Kasera, Mritunjay; Laha, Debabrata; Giehl, Ricardo F. H.; Schaaf, Gabriel & Bhattacharjee, Saikat
  
• ITPK1 is an InsP6/ADP phosphotransferase that controls phosphate signaling in Arabidopsis. Molecular Plant, 14(11), 1864-1880.
  Riemer, Esther; Qiu, Danye; Laha, Debabrata; Harmel, Robert K.; Gaugler, Philipp; Gaugler, Verena; Frei, Michael; Hajirezaei, Mohammad-Reza; Laha, Nargis Parvin; Krusenbaum, Lukas; Schneider, Robin; Saiardi, Adolfo; Fiedler, Dorothea; Jessen, Henning J.; Schaaf, Gabriel & Giehl, Ricardo F.H.
  
• Metal crossroads in plants: modulation of nutrient acquisition and root development by essential trace metals. Journal of Experimental Botany, 73(6), 1751-1765.
  Lešková, Alexandra; Javot, Hélène & Giehl, Ricardo F. H.
  
• Arabidopsis PFA-DSP-Type Phosphohydrolases Target Specific Inositol Pyrophosphate Messengers. Biochemistry, 61(12), 1213-1227.
  Gaugler, Philipp; Schneider, Robin; Liu, Guizhen; Qiu, Danye; Weber, Jonathan; Schmid, Jochen; Jork, Nikolaus; Häner, Markus; Ritter, Kevin; Fernández-Rebollo, Nicolás; Giehl, Ricardo F. H.; Trung, Minh Nguyen; Yadav, Ranjana; Fiedler, Dorothea; Gaugler, Verena; Jessen, Henning J.; Schaaf, Gabriel & Laha, Debabrata
  
• INOSITOL (1,3,4) TRIPHOSPHATE 5/6 KINASE1-dependent inositol polyphosphates regulate auxin responses in Arabidopsis. Plant Physiology, 190(4), 2722-2738.
  Laha, Nargis Parvin; Giehl, Ricardo F H; Riemer, Esther; Qiu, Danye; Pullagurla, Naga Jyothi; Schneider, Robin; Dhir, Yashika Walia; Yadav, Ranjana; Mihiret, Yeshambel Emewodih; Gaugler, Philipp; Gaugler, Verena; Mao, Haibin; Zheng, Ning; von Wirén, Nicolaus; Saiardi, Adolfo; Bhattacharjee, Saikat; Jessen, Henning J; Laha, Debabrata & Schaaf, Gabriel
  
• Involvement of NGATHA-Like 1 Transcription Factor in Boron Transport under Low and High Boron Conditions. Plant and Cell Physiology, 63(9), 1242-1252.
  Tsednee, Munkhtsetseg; Tanaka, Mayuki; Giehl, Ricardo Fh; von, Wirén Nicolaus & Fujiwara, Toru