Cross species multi-omics reveals cell wall sequestration and elevated global transcription as mechanisms of boron tolerance in plants

Abstract

Boron toxicity is a worldwide problem for crop production, yet we have only a limited understanding of the genetic responses and adaptive mechanisms to this environmental stress in plants. Here we identified responses to excess boron in boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte relative Schrenkiella parvula using comparative genomics, transcriptomics, metabolomics, and ionomics. S. parvula maintains a lower level of total boron and free boric acid in its roots and shoots and sustains growth for longer durations than A. thaliana when grown with excess boron. S. parvula likely excludes boron more efficiently than A. thaliana, which we propose is partly driven by BOR5, a boron transporter that we functionally characterized in the current study. Both species allocate significant transcriptomic and metabolomic resources to enable their cell walls to serve as a partial sink for excess boron, particularly discernable in A. thaliana shoots. We provide evidence that the S. parvula transcriptome is pre-adapted to boron toxicity, exhibiting substantial overlap with the boron-stressed transcriptome of A. thaliana. Our transcriptomic and metabolomics data also suggest that RNA metabolism is a primary target of boron toxicity. Cytoplasmic boric acid likely forms complexes with ribose and ribose-containing compounds critical to RNA and other primary metabolic functions. A model depicting some of the cellular responses that enable a plant to grow in the presence of normally toxic levels of boron is presented.

Positive Selection and Heat-Response Transcriptomes Reveal Adaptive Features of the Brassicaceae Desert Model, Anastatica hierochuntica

“…Overall, our data show that: (i) A. thaliana and A. hierochuntica exhibit similar transcriptional adjustment; (ii) a large majority of orthologs display a shared response mode unlike the extremophyte S. parvula response to boron toxicity where almost no genes showed a shared response (Wang et al, 2020); (iii) only a few hundred orthologs in both species show a stress-ready mode of expression. These findings suggest that A. hierochuntica does not display the classic features of a stress-ready transcriptome (Kazachkova et al, 2018;Wang et al, 2021).…”

“…The distinction between A. hierochuntica and the other extremophyte relatives was further illustrated by our finding that the A. hierochuntica transcriptome behaves very differently in response to stress. The extent of transcriptomic, proteomic and metabolic adjustment of the halophytes E. salsugineum and S. parvula in response to ionic stress is much lower than that of A. thaliana (Taji et al, 2004;Gong et al, 2005;Lugan et al, 2010;Pang et al, 2010;Oh et al, 2014;Vera-Estrella et al, 2014;Kazachkova et al, 2018;Wang et al, 2021). In contrast, A. thaliana and A. hierochuntica exhibit similar transcriptome adjustment in response to heat stress and during recovery (Figs.…”

“…it does not exist in a stress-ready state. To further test this hypothesis, we used Weighted Gene Co-expression Network Analysis (WGCNA; Langfelder and Horvath, 2008) to identify five types of transcriptional response mode among the expression patterns of 17,962 orthologous pairs for each species (Wang et al, 2021;Supplemental Fig. S5; Supplemental Table S13): (a) "Stress-ready" where transcript level under control conditions in one species is equal to the ortholog transcript level under heat in the other species;…”

“…For example, the halophyte models Eutrema salsugineum and Schrenkiella parvula, have revealed that differences between salt-sensitive and salt-tolerant relatives are associated with altered regulation of basic physiological and molecular processes including: (i) global pre-adaptation to stress, which is manifest as reduced adjustment of the transcriptome, proteome, and metabolome in response to a stress challenge compared to A. thaliana, and constitutively high or low expressed genes in the halophytes that are induced or repressed, respectively, in stress-sensitive plants. In other words, these halophytes appear to exist in a stress-ready state even under stress-neutral conditions (Taji et al, 2004;Kant et al, 2006;Kant et al, 2008a;Lugan et al, 2010;Pang et al, 2010;Kazachkova et al, 2013;Oh et al, 2014;Wang et al, 2021); (ii) E. salsugineum is able to maintain energy supply under saline conditions via alternative pathways acting as sinks for excess electrons and via protection of chloroplasts by a highly active ROS-scavenging system (Stepien and Johnson, 2009;Wiciarz et al, 2015;Pilarska et al, 2016); (iii) at the genome level, structural changes have led to the selective expansion (e.g. tandem duplication) of genes with subfuctionalization and/or neofuctionalization leading to changes in expression and/or function (Sun et al, 2010;Dassanayake et al, 2011a;Dassnayake et al, 2011b;Ali et al, 2012;Oh et al, 2014;Ali et al, 2016;Ali et al, 2018; The tree contains five extremophyte species considered to be naturally tolerant to various abiotic stresses (Fig 2A,red asterisks): the halophytes Eutrema salsugineum and Schrenkiella parvula (tolerant to high salinity and multiple other stresses; Kazachkova et al, 2018), Thlaspi arvense (freezing-tolerant; Sharma et al, 2007;Zhou et al, 2007), A. hierochuntica (heat-, salt-, low N-tolerant;Eshel et al, 2017) and Arabidopsis halleri (heavy metal hyperaccumulator, semi-alpine conditions; Hanikenne et al, 2008;Honjo and Kudoh, 2019).…”

Assessing Yield Response and Relationship of Soil Boron Fractions with Its Accumulation in Sorghum and Cowpea under Boron Fertilization in Different Soil Series

“…It is well-known that in all agricultural areas, the natural B content in soil or irrigation water may cause B toxicity, especially when the water originates near active geothermal areas. B-induced toxicity can adversely affect physiological attributes and yield of crops [48,49]. In addition, high levels of B toxicity occur in arid and semi-arid environments, and high salinity can increase crop stress [50].…”