Transcriptome analysis of the phosphate starvation response sheds light on strigolactone biosynthesis in rice

Abstract

SUMMARY Phosphorus (P) is a major element required for plant growth and development. To cope with P shortage, plants activate local and long‐distance signaling pathways, such as an increase in the production and exudation of strigolactones (SLs). The role of the latter in mitigating P deficiency is, however, still largely unknown. To shed light on this, we studied the transcriptional response to P starvation and replenishment in wild‐type rice and a SL mutant, dwarf10 (d10), and upon exogenous application of the synthetic SL GR24. P starvation resulted in major transcriptional alterations, such as the upregulation of P TRANSPORTER, SYG1/PHO81/XPR1 (SPX) and VACUOLAR PHOSPHATE EFFLUX TRANSPORTER. Gene Ontology (GO) analysis of the genes induced by P starvation showed enrichment in phospholipid catabolic process and phosphatase activity. In d10, P deficiency induced upregulation of genes enriched for sesquiterpenoid production, secondary shoot formation and metabolic processes, including lactone biosynthesis. Furthermore, several genes induced by GR24 treatment shared the same GO terms with P starvation‐induced genes, such as oxidation reduction, heme binding and oxidoreductase activity, hinting at the role that SLs play in the transcriptional reprogramming upon P starvation. Gene co‐expression network analysis uncovered a METHYL TRANSFERASE that displayed co‐regulation with known rice SL biosynthetic genes. Functional characterization showed that this gene encodes an enzyme catalyzing the conversion of carlactonoic acid to methyl carlactonoate. Our work provides a valuable resource to further studies on the response of crops to P deficiency and reveals a tool for the discovery of SL biosynthetic genes.

MASCARA: coexpression analysis in data from designed experiments

“…At each combination of growth condition and time point, the root transcriptome of three new plants was harvested for RNA sequencing. In this dataset, the curated list of SL pathway genes (contained in Supplementary Table 1) shows a specific profile: low variance baseline expression across all time points in the P+ condition but activation and increasing expression over time with P starvation, data were generated and preprocessed to variance stabilised counts as per (5).…”

“…The interaction between these two pathways has been characterised recently under nitrogen limitation by (24). transformed expression level of one of the bait genes (CCD8), y axes; expression levels of three example coexpression candidates for each method (see (5) for preprocessing details).…”

Chromosome-scale pearl millet genomes reveal aCARLACTONOIC ACID METHYL TRANSFERASEas key determinant of strigolactone pattern and Striga susceptibility

“…The homologues of SL biosynthetic genes in pearl millet PgD27 ( PgP10c0101G011332 ), PgCCD8 ( PgP10c0601G021829 ), PgMAX1 - 1400 ( PgP10c0601G022366 ), PgCYP706 ( PgP10c0401G051155 ) and PgCLAMT1b ( PgP10c0201G045110 ) (Supplementary figures 8, 9, 10) were all markedly upregulated in P10 under low Pi conditions (over 32-fold) and further by MP3 treatment. The canonical SL analog GR24 suppresses SL biosynthetic genes in rice, even under Pi deficiency (Haider et al, 2023). Therefore, the unexpected increase in expression observed here may be because MP3, a non-canonical SL analog, acts differently from GR24, or because SL biosynthesis is regulated differently in pearl millet compared to rice.…”

“…Notably, CLAMT1b was absent in the Aw genome, as were CLAMT1c ( PgP10c0201G045096.1 ), a CYP51 homolog and a putative acyl transferase encoded by the 0.7 Mb fragment present in P10 (Figure 2b). CLAMT enzymes, involved in SL biosynthesis in rice and maize (Haider et al, 2023; Li et al, 2023), convert carlactonoic acid (CLA) into methyl carlactonoate (MeCLA) (Mashiguchi et al, 2022) in the formation of non-canonical SLs. In pearl millet, we identified three CLAMT genes with differing responses to phosphate starvation and MP3 treatment.…”

Integration of Apocarotenoid Profile and Expression Pattern ofCarotenoid Cleavage Dioxygenasesduring Mycorrhization in Rice

“…It has been recently shown that a complex gene network centered on the plant Pi starvation response actively supervises AM fungal development in roots, acting at the local and systemic level (Shi et al ., 2021; Das et al ., 2022). Pi starvation also induces SL biosynthesis and release (Yoneyama et al ., 2007; Wang et al ., 2017, 2022), while high Pi levels repress the expression of genes involved in the biosynthesis of carotenoids and SLs in root (Carbonnel and Gutjahr, 2014; Haider et al ., 2023). SLs are the best-known plant molecules active in the pre-symbiotic interaction with AM fungi.…”