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, 116 (11), 5015-5020

Evolution of Chloroplast Retrograde Signaling Facilitates Green Plant Adaptation to Land

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Evolution of Chloroplast Retrograde Signaling Facilitates Green Plant Adaptation to Land

Chenchen Zhao et al. Proc Natl Acad Sci U S A.

Abstract

Chloroplast retrograde signaling networks are vital for chloroplast biogenesis, operation, and signaling, including excess light and drought stress signaling. To date, retrograde signaling has been considered in the context of land plant adaptation, but not regarding the origin and evolution of signaling cascades linking chloroplast function to stomatal regulation. We show that key elements of the chloroplast retrograde signaling process, the nucleotide phosphatase (SAL1) and 3'-phosphoadenosine-5'-phosphate (PAP) metabolism, evolved in streptophyte algae-the algal ancestors of land plants. We discover an early evolution of SAL1-PAP chloroplast retrograde signaling in stomatal regulation based on conserved gene and protein structure, function, and enzyme activity and transit peptides of SAL1s in species including flowering plants, the fern Ceratopteris richardii, and the moss Physcomitrella patens Moreover, we demonstrate that PAP regulates stomatal closure via secondary messengers and ion transport in guard cells of these diverse lineages. The origin of stomata facilitated gas exchange in the earliest land plants. Our findings suggest that the conquest of land by plants was enabled by rapid response to drought stress through the deployment of an ancestral SAL1-PAP signaling pathway, intersecting with the core abscisic acid signaling in stomatal guard cells.

Keywords: comparative genomics; green plant evolution; signal transduction; stomata; water stress.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Evolutionary similarity of protein families of the major clades of green plants. (A) Similarity heat map for the evolution of protein families of sulfur metabolism, ROS and NO signaling, photoreceptors, and protein kinases. A simplified tree is shown and color-coded to the main clades of Viridiplantae (green plants). (B) Comparative genetic similarity analysis was conducted with protein sequences of 31 plant and algal species that span the green plant kingdom from chlorophytes to angiosperms. Sulfur metabolism (n = 11), ROS and NO signaling (n = 19), membrane transporters (n = 20), ABA receptors (n = 3), photoreceptors (n = 5), protein kinases (n = 3). Different lowercase letters indicate statistical significance at P < 0.05. Genesis software (genome.tugraz.at/genesisclient/genesisclient_download.shtml) was used to estimate the similarity of proteins using A. thaliana sequences as the query with the criterion of E-value < 10−5. Colored squares: 0 (yellow), 100% (green), no proteins satisfied the selection criterion (gray). For abbreviations, see SI Appendix, Table S1.
Fig. 2.
Fig. 2.
Bioinformatics analysis of SAL1s and their transit peptides in streptophyte species and cloning and functional analysis of SAL1s of C. richardii and P. patens. (A) Phylogenetic tree of SAL1s using key species of the major green plant and algal clades of the 1KP database (www.onekp.com). Phylogenetic tree with all of the SAL1s is in SI Appendix, Fig. S2D. (B) Alignment of the SAL1 transit peptides and partial mature protein in different species. Representative sequences are obtained from expressed mRNAs of different lineage groups. Alignment and sequence logos were conducted for only the first 30 amino acids of the SAL1 mature protein conserved region. At, A. thaliana; Co, C. orbicularis; Cr, C. richardii; Hv, H. vulgare; Mp, M. polymorpha; Nm, Nitella mirabilis; Pl, Pinus lambertiana; Pp, P. patens; Zc, Z. circumcarinatum. (C and D) CrSAL1 and PpSAL1 activity (pmol AMP⋅µg−1protein⋅min−1) assay against 25 and 200 μM PAP in the presence of different SAL1 activity regulators including cofactor (Mg2+), active site inhibitor (Li+), redox activator (DTTred), and redox inhibitor (DTTox) (n = 3). The “+” and “−” signs represent with or without the regulators, respectively, in the corresponding reactions. **P < 0.01.
Fig. 3.
Fig. 3.
PAP-induced stomatal closure, guard-cell ROS and NO signaling, and ion transport are evolutionarily conserved across plant clades. (A) Stomatal aperture (pore aperture for M. polymorpha) at 0 and 120 min after PAP treatment. Data are means ± SE (n = 5–7 biological replicates, 30–80 stomata/pores). (B and C) PAP induces H2O2 [2′,7′-dichlorodihydrofluorescein diacetate (H2DCFDA)] and NO [diaminofluorescein diacetate (DAF-2DA)] production in guard cells of plants from across three major clades measured in the control and after 50 min in 100 µM PAP. Data are means ± SE (n = 5 with 50–100 guard cells). (Scale bars, 10 μm.) (DF) PAP regulates K+, Cl, and Ca2+ fluxes from guard cells of three major clades. Data are averaged for control (0–10 min) and PAP (15–35 min). Data are means ± SE (n = 5–8). (G) PAP activates plasma membrane Ca2+ and anion channels in guard cells of A. thaliana. Average steady-state Ca2+ channel currents at −100 mV and anion channel currents at −200 mV in the control and 15 min after adding 100 μM PAP to the bath solution. Data are means ± SE (n = 4–10). *P < 0.05, **P < 0.01. (H) Schematic diagram of potential PAP-induced signal transduction in guard cells. Arrows: activation (blue), inhibition (purple), direction of ion and PAP movement (red), Ca2+ rise (green).

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