The rubisco chaperone BSD2 may regulate chloroplast coverage in maize bundle sheath cells

Coralie Salesse, Robert Sharwood, Wataru Sakamoto, David Stern

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

In maize (Zea mays), Bundle Sheath Defective2 (BSD2) plays an essential role in Rubisco biogenesis and is required for correct bundle sheath (BS) cell differentiation. Yet, BSD2 RNA and protein levels are similar in mesophyll (M) and BS chloroplasts, although Rubisco accumulates only in BS chloroplasts. This raises the possibility of additional BSD2 roles in cell development. To test this hypothesis, transgenic lines were created that overexpress and underexpress BSD2 in both BS and M cells, driven by the cell type-specific Rubisco Small Subunit (RBCS) or Phosphoenolpyruvate Carboxylase (PEPC) promoters or the ubiquitin promoter. Genetic crosses showed that each of the transgenes could complement Rubisco deficiency and seedling lethality conferred by the bsd2 mutation. This was unexpected, as RBCS-BSD2 lines lacked BSD2 in M chloroplasts and PEPC-BSD2 lines expressed half the wild-type BSD2 level in BS chloroplasts.We conclude that BSD2 does not play a vital role inM cells and that BS BSD2 is in excess of requirements for Rubisco accumulation. BSD2 levels did affect chloroplast coverage in BS cells. In PEPC-BSD2 lines, chloroplast coverage decreased 30% to 50%, whereas lines with increased BSD2 content exhibited a 25% increase. This suggests that BSD2 has an ancillary role in BS cells related to chloroplast size. Gas exchange showed decreased photosynthetic rates in PEPC-BSD2 lines despite restored Rubisco function, correlating with reduced chloroplast coverage and pointing to CO2 diffusion changes. Conversely, increased chloroplast coverage did not result in increased Rubisco abundance or photosynthetic rates. This suggests another limitation beyond chloroplast volume, most likely Rubisco biogenesis and/or turnover rates.

Original languageEnglish
Pages (from-to)1624-1633
Number of pages10
JournalPlant Physiology
Volume175
Issue number4
DOIs
Publication statusPublished - Dec 1 2017

Fingerprint

Ribulose-Bisphosphate Carboxylase
bundle sheath cells
ribulose-bisphosphate carboxylase
Chloroplasts
Zea mays
chloroplasts
corn
Phosphoenolpyruvate Carboxylase
phosphoenolpyruvate carboxylase
Genetic Crosses
promoter regions
cells
ubiquitin
Ubiquitin
Transgenes
Seedlings
cell differentiation
mesophyll
transgenes
gas exchange

ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

Cite this

The rubisco chaperone BSD2 may regulate chloroplast coverage in maize bundle sheath cells. / Salesse, Coralie; Sharwood, Robert; Sakamoto, Wataru; Stern, David.

In: Plant Physiology, Vol. 175, No. 4, 01.12.2017, p. 1624-1633.

Research output: Contribution to journalArticle

Salesse, Coralie ; Sharwood, Robert ; Sakamoto, Wataru ; Stern, David. / The rubisco chaperone BSD2 may regulate chloroplast coverage in maize bundle sheath cells. In: Plant Physiology. 2017 ; Vol. 175, No. 4. pp. 1624-1633.
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abstract = "In maize (Zea mays), Bundle Sheath Defective2 (BSD2) plays an essential role in Rubisco biogenesis and is required for correct bundle sheath (BS) cell differentiation. Yet, BSD2 RNA and protein levels are similar in mesophyll (M) and BS chloroplasts, although Rubisco accumulates only in BS chloroplasts. This raises the possibility of additional BSD2 roles in cell development. To test this hypothesis, transgenic lines were created that overexpress and underexpress BSD2 in both BS and M cells, driven by the cell type-specific Rubisco Small Subunit (RBCS) or Phosphoenolpyruvate Carboxylase (PEPC) promoters or the ubiquitin promoter. Genetic crosses showed that each of the transgenes could complement Rubisco deficiency and seedling lethality conferred by the bsd2 mutation. This was unexpected, as RBCS-BSD2 lines lacked BSD2 in M chloroplasts and PEPC-BSD2 lines expressed half the wild-type BSD2 level in BS chloroplasts.We conclude that BSD2 does not play a vital role inM cells and that BS BSD2 is in excess of requirements for Rubisco accumulation. BSD2 levels did affect chloroplast coverage in BS cells. In PEPC-BSD2 lines, chloroplast coverage decreased 30{\%} to 50{\%}, whereas lines with increased BSD2 content exhibited a 25{\%} increase. This suggests that BSD2 has an ancillary role in BS cells related to chloroplast size. Gas exchange showed decreased photosynthetic rates in PEPC-BSD2 lines despite restored Rubisco function, correlating with reduced chloroplast coverage and pointing to CO2 diffusion changes. Conversely, increased chloroplast coverage did not result in increased Rubisco abundance or photosynthetic rates. This suggests another limitation beyond chloroplast volume, most likely Rubisco biogenesis and/or turnover rates.",
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