Cross species multi‐omics reveals cell wall sequestration and elevated global transcript abundance as mechanisms of boron tolerance in plants

Abstract

Boron toxicity is a world-wide problem for crops, yet we have a limited understanding of the genetic responses and adaptive mechanisms to this stress in plants.We employed a cross-species comparison between boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte relative Schrenkiella parvula, and a multiomics approach integrating genomics, transcriptomics, metabolomics and ionomics to assess plant responses and adaptations to boron stress.Schrenkiella parvula maintains lower concentrations of total boron and free boric acid than Arabidopsis when grown with excess boron. Schrenkiella parvula excludes excess boron more efficiently than Arabidopsis, which we propose is partly driven by SpBOR5, a boron transporter that we functionally characterize in this study. Both species use cell walls as a partial sink for excess boron. When accumulated in the cytoplasm, excess boron appears to interrupt RNA metabolism. The extremophyte S. parvula facilitates critical cellular processes while maintaining the pool of ribose-containing compounds that can bind with boric acid.The S. parvula transcriptome is pre-adapted to boron toxicity. It exhibits substantial overlaps with the Arabidopsis boron-stress responsive transcriptome. Cell wall sequestration and increases in global transcript levels under excess boron conditions emerge as key mechanisms for sustaining plant growth under boron toxicity.

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 stressready 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).…”

“…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 9 one species is equal to the ortholog transcript level under heat in the other species; (b) "Shared response" where expression of both orthologs exhibit a similar response to heat; (c) "Unique response" where expression of an ortholog exhibits a heat response specifically in one species but not in the other; (d) "Opposite response" where expression of the ortholog in one species shows the opposite response in the other species; (e) "No response" where the expression of both orthologs does not respond to heat.…”

“…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.…”

“…The lower transcriptomic and metabolic adjustment of the halophytic relatives is reflected in their stress-ready state in stress-neutral conditions whereby transcript and metabolite accumulation that is induced or repressed in A. thaliana in response to ionic stress, exhibits constitutively high or low accumulation, respectively, in the halophytes (Gong et al, 2005;Lugan et al, 2010;Kazachkova et al, 2013;Oh et al, 2014;Kazachkova et al, 2018;Wang et al, 2021). For instance, S. parvula possesses a pre-boron stressadapted genome with over 1,000 stress-ready orthologs whose basal expression levels match the poststress expression levels observed in A. thaliana (Wang et al, 2021). No boron stress-ready A. thaliana orthologs were detected and there were almost no orthologs showing a shared response to excess boron.…”

Carbon-11 Radiotracing Reveals Physiological and Metabolic Responses of Maize Grown under Different Regimes of Boron Treatment

“…Moreover, the negative effects of boron-deficient and boron-toxic conditions on plant photosynthesis (as reviewed in [ 5 , 42 , 43 ]), with widespread impacts on carbohydrate and amino acid metabolism [ 44 , 45 , 46 , 47 , 48 ], have been reported for other species. Even so, the mechanisms underlying these effects are unclear.…”