Network Inference of Transcriptional Regulation in Germinating Low Phytic Acid Soybean Seeds

Abstract

The low phytic acid (lpa) trait in soybeans can be conferred by loss-of-function mutations in genes encoding myo-inositol phosphate synthase and two epistatically interacting genes encoding multidrug-resistance protein ATP-binding cassette (ABC) transporters. However, perturbations in phytic acid biosynthesis are associated with poor seed vigor. Since the benefits of the lpa trait, in terms of end-use quality and sustainability, far outweigh the negatives associated with poor seed performance, a fuller understanding of the molecular basis behind the negatives will assist crop breeders and engineers in producing variates with lpa and better germination rate. The gene regulatory network (GRN) for developing low and normal phytic acid soybean seeds was previously constructed, with genes modulating a variety of processes pertinent to phytic acid metabolism and seed viability being identified. In this study, a comparative time series analysis of low and normal phytic acid soybeans was carried out to investigate the transcriptional regulatory elements governing the transitional dynamics from dry seed to germinated seed. GRNs were reverse engineered from time series transcriptomic data of three distinct genotypic subsets composed of lpa soybean lines and their normal phytic acid sibling lines. Using a robust unsupervised network inference scheme, putative regulatory interactions were inferred for each subset of genotypes. These interactions were further validated by published regulatory interactions found in Arabidopsis thaliana and motif sequence analysis. Results indicate that lpa seeds have increased sensitivity to stress, which could be due to changes in phytic acid levels, disrupted inositol phosphate signaling, disrupted phosphate ion (Pi) homeostasis, and altered myo-inositol metabolism. Putative regulatory interactions were identified for the latter two processes. Changes in abscisic acid (ABA) signaling candidate transcription factors (TFs) putatively regulating genes in this process were identified as well. Analysis of the GRNs reveal altered regulation in processes that may be affecting the germination of lpa soybean seeds. Therefore, this work contributes to the ongoing effort to elucidate molecular mechanisms underlying altered seed viability, germination and field emergence of lpa crops, understanding of which is necessary in order to mitigate these problems.

Rice ins(3)P synthase1 (RINO1) participates in embryonic development by regulating inositol‐associated changes in auxin synthesis and its distribution

“…Nutritional surveys of humans have demonstrated that LPA crops can enhance the bioavailability of iron, zinc, and calcium (Perera et al, 2018; Dong & Saneoka, 2020). Unfortunately, the LPA mutant crops with reduced InsP 6 content usually exhibit inferior seed vigour and lower seedling emergence than their normal InsP 6 counterparts (Nunes et al, 2006; Zhao et al, 2008; Naidoo et al, 2012; Zhou et al, 2018; Demers et al, 2021; Oo et al, 2023). Therefore, great attention has been paid to the relationship of inferior seed performance and yield loss with the marked reduction of grain InsP 6 content in LPA crops.…”

“…Suppressed expression of RINO1 through RNAi significantly reduces the InsP 6 content in mature rice seeds (Kuwano et al, 2009; Ali et al, 2013). Beyond seed InsP 6 biosynthesis, MIPS expression and its relevant metabolites play essential roles in various developmental processes across plant tissues (Chen & Xiong, 2010; Luo et al, 2011; Demers et al, 2021). The perturbation of InsP 6 synthesis due to MIPS suppression negatively affects seed germination and seedling emergence in many plant species (Raboy, 2009; Kuwano et al, 2009; Zhou et al, 2018).…”

“…The null MIPS1 mutations in Arabidopsis cause multiple defects in embryogenesis, cotyledon vein patterning, epidermal cell division, root growth, root gravitropism, root cap cell patterning, apical dominance, and auxin response. (Chen & Xiong, 2010; Mei et al, 2012; Demers et al, 2021). The maize LPA mutant ( lpa‐241 ) with reduced MIPS expression shows defects in embryo development and seed germination (Pilu et al, 2005).…”

“…Myo ‐inositol serves as the substrate for synthesizing phosphatidylinositol (PI) and phosphatidylinositides (PIs) (Guttieri et al, 2004; Suzuki et al, 2007), with PIs constituting 21% of the phospholipids in non‐photosynthetic plant membranes (Luo et al, 2011). Numerous studies have highlighted the essential roles of myo ‐inositol and its derivatives in various cellular, physiological and biochemical processes, such as signal transduction, mRNA export, hormone signalling, stress response, membrane permeability, and cell wall biogenesis (Chen & Xiong, 2010; Mei et al, 2012; Demers et al, 2021). The studies on Arabidopsis have revealed that myo‐inositol acts as a cofactor for auxin binding to the TIR1 auxin receptor (Mei et al, 2012).…”

Isoflavones Play a Potential Role in Off-Flavour Scavenging, with a Key Role of IFS2 in Isoflavone Accumulation in Soybean Seeds

“…The phytates are essential for phosphate storage and act as feeding deterrents. Therefore, concerns remain regarding their harmful effect on plant survival ( 5 ).…”