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Evolution of an intermediate C4 photosynthesis in the non-foliar tissues of the Poaceae

Abstract

Carbon concentrating mechanisms (CCMs) in plants are abaptive features that have evolved to sustain plant growth in unfavorable environments, especially at low atmospheric carbon levels and high temperatures. Uptake of CO2 and its storage in the aerenchyma tissues of Lycopsids and diurnal acidity fluctuation in aquatic plants during the Palaeozoic era (ca. 300 Ma.) would represent the earliest evolution of a CCM. The CCM parts of the dark reactions of photosynthesis have evolved many times, while the light reactions are conserved across plant lineages. A C4 type CCM, leaf C4 photosynthesis is evolved in the PACMAD clade of the Poaceae family. The evolution of C4 photosynthesis from C3 photosynthesis was an abaptation. Photosynthesis in reproductive tissues of sorghum and maize (PACMAD clade) has been shown to be of a weaker C4 type (high CO2 compensation point, low carbon isotope discrimination, and lack of Rubisco compartmentalization, when compared to the normal C4 types) than that in the leaves (normal C4 type). However, this does not fit well with the character polarity concept from an evolutionary perspective. In a recent model proposed for CCM evolution, the development of a rudimentary CCM prior to the evolution of a more efficient CCM (features contrasting to a weaker C4 type, leading to greater biomass production rate) has been suggested. An intermediate crassulacean acid metabolism (CAM) type of CCM (rudimentary) was reported in the genera, Brassia, Coryanthes, Eriopsis, Peristeria, of the orchids (well-known group of plants that display the CAM pathway). Similarly, we propose here the evolution of a rudimentary CCM (C4-like type pathway) in the non-foliar tissues of the Poaceae, prior to the evolution of the C4 pathway as identified in the leaves of the C4 species of the PACMAD clade.

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Fig. 1

Data availability

The data pertaining to the discussion in this study, developed by the author is available for access in the public domain (E-MTAB-8361 / PRJEB34534).

Code availability

Not applicable.

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Acknowledgements

The authors acknowledge the Indian Council of Agricultural Research, New Delhi for the research grant 16113160001-1006976 under the ‘Incentivizing research in Agriculture’ scheme. The authors are grateful to Govindjee Govindjee (of the University of Illinois at Urbana-Champaign, USA) and the anonymous reviewers, for their critical inputs, comments, and suggestions.

Funding

Indian Council of Agricultural Research, New Delhi (16113160001–1006976).

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Investigation and formal analysis, Parimalan Rangan, Rajkumar Subramani, Dhammaprakash Wankhede, Viswanathan Chinnusamy and Kuldeep Singh; Funding acquisition, Surendra Malik and Mirza Jaynul Baig; Supervision, Conceptualization and hypothesis, Parimalan Rangan; Writing – original draft, Parimalan Rangan; Writing – review & editing, Parimalan Rangan, Robert Henry, Dhammaprakash Wankhede, Rajkumar Subramani, Viswanathan Chinnusamy, Surendra Malik, Mirza Jaynul Baig and Kuldeep Singh.

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Correspondence to Parimalan Rangan.

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Rangan, P., Wankhede, D.P., Subramani, R. et al. Evolution of an intermediate C4 photosynthesis in the non-foliar tissues of the Poaceae. Photosynth Res (2022). https://doi.org/10.1007/s11120-022-00926-7

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Keywords

  • Biochemical rewiring
  • Crassulacean acid metabolism
  • Abaptation
  • High temperature
  • Neo-functionalization
  • Non-foliar photosynthesis