Distinct C<sub>4</sub> sub‐types and C<sub>3</sub> bundle sheath isolation in the Paniceae grasses

Washburn, Jacob D.; Strable, Josh; Dickinson, Patrick; Kothapalli, Satya S.; Brose, Julia M.; Covshoff, Sarah; Conant, Gavin C.; Hibberd, Julian M.; Pires, J. Chris

doi:10.1002/pld3.373

Cited by 5 publications

(6 citation statements)

References 91 publications

(173 reference statements)

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“…Transcript expression associated with sugar-sensing genes was analysed within bundle sheath and mesophyll cells of several C 4 grasses from publicly available RNA-Seq datasets ( John et al , 2014 ; Döring et al , 2016 ; Denton et al , 2017 ; Washburn et al , 2021 ). These results are presented for Z. mays , S. bicolor , S. viridis , S. italica and P. hallii ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“… Sugar sensor gene expression between bundle sheath and mesophyll cells of C 4 grasses: Z. mays (A), Sorghum bicolor (B), Setaria viridis (C), Setaria italica (D) and P. hallii (E) ( John et al , 2014 ; Döring et al , 2016 ; Denton et al , 2017 ; Washburn et al , 2021 ). (F) Heat map comparison of log 2 TPM means of bundle sheath and mesophyll expression in C 4 grasses.…”

Section: Resultsmentioning

confidence: 99%

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Spatial expression patterns of genes encoding sugar sensors in leaves of C4 and C3 grasses

et al. 2023

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Background and aims The mechanisms of sugar sensing in grasses, especially those using C4 photosynthesis, remains elusive despite being a large proportion of the world’s agricultural crops. We addressed this gap by comparing the expression of genes encoding components of sugar sensors in C3 and C4 grasses, with a focus on source tissues of C4 grasses. Given C4 plants evolved into a two-cell carbon fixation system, it was hypothesised this may have also changed how sugars were sensed. Methods For six C3 and eight C4 grasses, putative sugar sensor genes were identified for Target of Rapamycin (TOR), SNF1- related kinase 1 (SnRK1), Hexokinase (HXK) and those involved in the metabolism of the sugar sensing metabolite trehalose-6-phosphate (T6P) using publicly available RNA deep sequencing data. For several of these grasses, expression was compared in three ways: source (leaf) vs. sink (seed), along the gradient of the leaf, and bundle sheath vs. mesophyll cells. Key Results No positive selection of codons associated with the evolution of C4 photosynthesis was identified in sugar sensor proteins here. Expression of genes encoding sugar sensors were relatively ubiquitous between source and sink tissues as well as along the leaf gradient of both C4 and C3 grasses. Across C4 grasses, SnRK1β1 and TPS1 were preferentially expressed in the mesophyll and bundle sheath cells, respectively. Species specific differences of gene expression between the two cell types were also apparent. Conclusions This comprehensive transcriptomic study provides an initial foundation for elucidating sugar sensing genes within major C4 and C3 crops. This study provides some evidence that C4 and C3 grasses do not differ in how sugars are sensed. While sugar sensor gene expression has a degree of stability along the leaf, there are some contrasts between the mesophyll and bundle sheath cells.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Spatial expression patterns of genes encoding sugar sensors in leaves of C4 and C3 grasses

et al. 2023

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“…In maize (NADP-ME subtype), carbon is primarily fixed as Mal, but significant pools (~25% of the fixed carbon) and rapid labelling of Asp have also been observed ( Hatch 1971 ; Meister et al 1996 ; Wingler et al 1999 ; Majeran et al 2010 ; Pick et al 2011 ; Muhaidat and McKown 2013 ; Weissmann et al 2015 ; Arrivault et al 2017 ). Furthermore, PEPCK is expressed in the BSC of the NADP-ME subtype and supports Asp-dependent photosynthesis in isolated BSC ( Chapman et al 1980 ; Chapman and Hatch 1981 ; Walker et al 1997 ; Wingler et al 1999 ; Majeran et al 2010 ; Pick et al 2011 ; Washburn et al 2021 ). It has been suggested that Asp decarboxylation varies with developmental and environmental conditions ( Chapman and Hatch 1981 ; Furbank 2011 ).…”

Section: Introductionmentioning

confidence: 84%

Integrating multiple regulations on enzyme activity: the case of phosphoenolpyruvate carboxykinases

Rojas

Iglesias

2023

AoB PLANTS

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Data on protein posttranslational modifications (PTMs) increased exponentially in the last years due to the refinement of mass spectrometry techniques and the development of databases to store and share datasets. Nevertheless, these data per se do not create comprehensive biochemical knowledge. Complementary studies on protein biochemistry are necessary to fully understand the function of these PTMs at the molecular level and beyond, for example, designing rational metabolic engineering strategies to improve crops. Phosphoenolpyruvate carboxykinases (PEPCKs) are critical enzymes for plant metabolism with diverse roles in plant development and growth. Multiple lines of evidence showed the complex regulation of PEPCKs, including PTMs. Herein, we present PEPCKs as an example of the integration of combined mechanisms modulating enzyme activity and metabolic pathways. PEPCKs studies strongly advanced after the production of the recombinant enzyme and the establishment of standardized biochemical assays. Finally, we discuss emerging open questions for future research and the challenges in integrating all available data into functional biochemical models.

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“…By contrast, an element of sub‐functionalization is apparent in the C 4 species maize and setaria, with the GLK2 paralog expressed preferentially in bundle sheath cells. However, data from a number of different C 3 , C 4, and intermediate species (Washburn et al., 2021 ) (Figure S1 ) invoke a more complex scenario because preferential expression of GLK2 paralogs in bundle sheath cells is evident in species where decarboxylation reactions occur in the bundle sheath chloroplasts (NADP‐ME type) but not in species where decarboxylation occurs in the mitochondria (NAD‐ME type) or in the cytoplasm (PEP‐CK type). This suggests that preferential localization of GLK2 in bundle sheath cells is associated with specific aspects of chloroplast function as opposed to general activation of photosynthesis.…”

Section: Discussionmentioning

confidence: 99%

GOLDEN2‐like1 is sufficient but not necessary for chloroplast biogenesis in mesophyll cells of C₄ grasses

Lambret‐Frotte,

Smith,

Langdale

2023

The Plant Journal

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SUMMARYChloroplasts are the site of photosynthesis. In land plants, chloroplast biogenesis is regulated by a family of transcription factors named GOLDEN2‐like (GLK). In C4 grasses, it has been hypothesized that genome duplication events led to the sub‐functionalization of GLK paralogs (GLK1 and GLK2) to control chloroplast biogenesis in two distinct cell types: mesophyll and bundle sheath cells. Although previous characterization of golden2 (g2) mutants in maize has demonstrated a role for GLK2 paralogs in regulating chloroplast biogenesis in bundle sheath cells, the function of GLK1 has remained elusive. Here we show that, contrary to expectations, GLK1 is not required for chloroplast biogenesis in mesophyll cells of maize. Comparisons between maize and Setaria viridis, which represent two independent C4 origins within the Poales, further show that the role of GLK paralogs in controlling chloroplast biogenesis in mesophyll and bundle sheath cells differs between species. Despite these differences, complementation analysis revealed that GLK1 and GLK2 genes from maize are both sufficient to restore functional chloroplast development in mesophyll and bundle sheath cells of S. viridis mutants. Collectively our results suggest an evolutionary trajectory in C4 grasses whereby both orthologs retained the ability to induce chloroplast biogenesis but GLK2 adopted a more prominent developmental role, particularly in relation to chloroplast activation in bundle sheath cells.

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Distinct C₄ sub‐types and C₃ bundle sheath isolation in the Paniceae grasses

Cited by 5 publications

References 91 publications

Spatial expression patterns of genes encoding sugar sensors in leaves of C4 and C3 grasses

Spatial expression patterns of genes encoding sugar sensors in leaves of C4 and C3 grasses

Integrating multiple regulations on enzyme activity: the case of phosphoenolpyruvate carboxykinases

GOLDEN2‐like1 is sufficient but not necessary for chloroplast biogenesis in mesophyll cells of C₄ grasses

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Distinct C4 sub‐types and C3 bundle sheath isolation in the Paniceae grasses

Cited by 5 publications

References 91 publications

Spatial expression patterns of genes encoding sugar sensors in leaves of C4 and C3 grasses

Spatial expression patterns of genes encoding sugar sensors in leaves of C4 and C3 grasses

Integrating multiple regulations on enzyme activity: the case of phosphoenolpyruvate carboxykinases

GOLDEN2‐like1 is sufficient but not necessary for chloroplast biogenesis in mesophyll cells of C4 grasses

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Distinct C₄ sub‐types and C₃ bundle sheath isolation in the Paniceae grasses

GOLDEN2‐like1 is sufficient but not necessary for chloroplast biogenesis in mesophyll cells of C₄ grasses