Whole Irradiated Plant Leaves Showed Faster Photosynthetic Induction Than Individually Irradiated Leaves via Improved Stomatal Opening

Rapid photosynthetic induction is crucial for plants under fluctuating light conditions in a crop canopy as well as in an understory. Most previous studies have focused on photosynthetic induction responses in a single leaf, whereas the systemic responses of the whole plant have not been considered. In a natural environment, however, both single leaves and whole plants are exposed to sunlight, since the light environment is not uniform even within a given plant. In the present study, we examined whether there is any difference between the photosynthetic induction response of a leaf of a whole irradiated plant and an individually irradiated leaf in Arabidopsis thaliana to consider photosynthetic induction as the response of a whole plant. We used two methods, the visualization of photosynthesis and direct measurements of gas-exchange and Chl fluorescence, to demonstrate that whole irradiated plant promoted its photosynthetic induction via improved stomatal opening compared with individually irradiated leaf. Furthermore, using two Arabidopsis knockout mutants of abscisic acid transporter, abcg25 and abcg40, the present study suggests that abscisic acid could be involved in this systemic response for stomatal opening, allowing plants to optimize the use of light energy at minimal cost in plants in a dynamic light environment.

[1]  Robert W. Pearcy,et al.  Sunfleck dynamics in relation to canopy structure in a soybean (Glycine max (L.) Merr.) canopy , 1990 .

[2]  R. W. Pearcy,et al.  Stomatal behavior and photosynthetic performance under dynamic light regimes in a seasonally dry tropical rain forest , 2000, Oecologia.

[3]  T. Kuromori,et al.  ABA Transport and Plant Water Stress Responses. , 2018, Trends in plant science.

[4]  O. Bethenod,et al.  Maize stomatal conductance in the field: its relationship with soil and plant water potentials, mechanical constraints and ABA concentration in the xylem sap , 1991 .

[5]  C. Tinoco-Ojanguren,et al.  Stomatal dynamics and its importance to carbon gain in two rainforest Piper species , 1993, Oecologia.

[6]  M. Moo-young,et al.  Ethanol fermentation technologies from sugar and starch feedstocks. , 2008, Biotechnology advances.

[7]  A. Portis Rubisco activase. , 1990, Biochimica et biophysica acta.

[8]  David M Kramer,et al.  Improving yield by exploiting mechanisms underlying natural variation of photosynthesis. , 2012, Current opinion in biotechnology.

[9]  Robert W. Pearcy,et al.  Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia , 1997 .

[10]  Annika E Huber,et al.  Long-distance plant signaling pathways in response to multiple stressors: the gap in knowledge. , 2016, Journal of experimental botany.

[11]  A. Leakey,et al.  High-temperature inhibition of photosynthesis is greater under sunflecks than uniform irradiance in a tropical rain forest tree seedling , 2003 .

[12]  J. Schroeder,et al.  Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis , 2014, Proceedings of the National Academy of Sciences.

[13]  Kun-song Chen,et al.  Systemic Induction of Photosynthesis via Illumination of the Shoot Apex Is Mediated Sequentially by Phytochrome B, Auxin and Hydrogen Peroxide in Tomato1[OPEN] , 2016, Plant Physiology.

[14]  Yin Wang,et al.  Overexpression of plasma membrane H+-ATPase in guard cells promotes light-induced stomatal opening and enhances plant growth , 2013, Proceedings of the National Academy of Sciences.

[15]  R. W. Pearcy,et al.  Two decades of sunfleck research: looking back to move forward. , 2012, Tree physiology.

[16]  A. Leakey,et al.  Physiological and ecological significance of sunflecks for dipterocarp seedlings. , 2004, Journal of experimental botany.

[17]  J. Christie,et al.  Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth , 2019, Science.

[18]  T. Kuromori,et al.  Intertissue Signal Transfer of Abscisic Acid from Vascular Cells to Guard Cells1[W] , 2014, Plant Physiology.

[19]  T. Givnish,et al.  Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: dynamic photosynthetic responses , 2008, Oecologia.

[20]  T. Shikanai,et al.  A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice , 2016, Scientific Reports.

[21]  P. Mullineaux,et al.  Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. , 1999, Science.

[22]  Ernst Steudle,et al.  A hydraulic signal in root-to-shoot signalling of water shortage. , 2007, The Plant journal : for cell and molecular biology.

[23]  J. Berry,et al.  Ion antiport accelerates photosynthetic acclimation in fluctuating light environments , 2014, Nature Communications.

[24]  R. Finkelstein,et al.  Abscisic Acid Signaling in Seeds and Seedlings Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010441. , 2002, The Plant Cell Online.

[25]  Tracy Lawson,et al.  Overexpression of the RieskeFeS Protein Increases Electron Transport Rates and Biomass Yield1[CC-BY] , 2017, Plant Physiology.

[26]  K. Solymosi,et al.  A voltage-dependent chloride channel fine-tunes photosynthesis in plants , 2016, Nature Communications.

[27]  Robert W. Pearcy,et al.  SUNFLECKS AND PHOTOSYNTHESIS IN PLANT CANOPIES , 1990 .

[28]  Kazuo Shinozaki,et al.  A small peptide modulates stomatal control via abscisic acid in long-distance signalling , 2018, Nature.

[29]  Xin-Guang Zhu,et al.  Improving photosynthetic efficiency for greater yield. , 2010, Annual review of plant biology.

[30]  T. Kuromori,et al.  ABC transporter AtABCG25 is involved in abscisic acid transport and responses , 2010, Proceedings of the National Academy of Sciences.

[31]  K. Ljung,et al.  Developmental regulation of indole-3-acetic acid turnover in Scots pine seedlings. , 2001, Plant physiology.

[32]  W. Yamori Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress , 2016, Journal of Plant Research.

[33]  I. E. Woodrow,et al.  Modelling the role of Rubisco activase in limiting non-steady-state photosynthesis. , 2000, Journal of experimental botany.

[34]  S. Long,et al.  Can improvement in photosynthesis increase crop yields? , 2006, Plant, cell & environment.

[35]  S. Jacobsen,et al.  Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. , 1996, The Plant journal : for cell and molecular biology.

[36]  E. Heuvelink,et al.  Metabolic and diffusional limitations of photosynthesis in fluctuating irradiance in Arabidopsis thaliana , 2016, Scientific Reports.

[37]  J. Giraudat Abscisic acid signaling. , 1995, Current opinion in cell biology.

[38]  R. Mittler,et al.  Evidence for the Involvement of Electrical, Calcium and ROS Signaling in the Systemic Regulation of Non-Photochemical Quenching and Photosynthesis , 2017, Plant & cell physiology.

[39]  J. Seemann,et al.  Photosynthetic induction state of leaves in a soybean canopy in relation to light regulation of ribulose-1-5-bisphosphate carboxylase and stomatal conductance. , 1990, Plant physiology.

[40]  M. Salvucci,et al.  The Regulatory Properties of Rubisco Activase Differ among Species and Affect Photosynthetic Induction during Light Transitions1[W][OA] , 2013, Plant Physiology.

[41]  U. Rascher,et al.  Functional dynamics of plant growth and photosynthesis--from steady-state to dynamics--from homogeneity to heterogeneity. , 2006, Plant, cell & environment.

[42]  K. Halliday,et al.  Integration of light and auxin signaling. , 2009, Cold Spring Harbor perspectives in biology.

[43]  H. Lichtenthaler,et al.  Induction of photosynthesis and importance of limitations during the induction phase in sun and shade leaves of five ecologically contrasting tree species from the temperate zone. , 2007, Tree physiology.

[44]  O. Bethenod,et al.  Xylem ABA controls the stomatal conductance of field‐grown maize subjected to soil compaction or soil drying , 1992 .

[45]  G. Krouk,et al.  ABA transport and transporters. , 2013, Trends in plant science.

[46]  Zishan Zhang,et al.  Systemic signalling in photosynthetic induction of Rumex K-1 (Rumex patientia × Rumex tianschaious) leaves. , 2015, Plant, cell & environment.

[47]  S. Adachi,et al.  Natural genetic variation of the photosynthetic induction response to fluctuating light environment. , 2019, Current opinion in plant biology.

[48]  Y. Kamiya,et al.  Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor , 2012, Proceedings of the National Academy of Sciences.

[49]  N. Baker Chlorophyll fluorescence: a probe of photosynthesis in vivo. , 2008, Annual review of plant biology.

[50]  Florian A. Busch,et al.  Strategies for Optimizing Photosynthesis with Biotechnology to Improve Crop Yield , 2016 .

[51]  S. Assmann,et al.  PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid , 2010, Proceedings of the National Academy of Sciences.

[52]  R. W. Pearcy,et al.  Stomatal versus biochemical limitations to dynamic photosynthetic performance in four tropical rainforest shrub species , 2000, Oecologia.

[53]  W. Yamori,et al.  Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. , 2012, The Plant journal : for cell and molecular biology.

[54]  I. Terashima,et al.  Enhanced leaf photosynthesis as a target to increase grain yield: insights from transgenic rice lines with variable Rieske FeS protein content in the cytochrome b6 /f complex. , 2016, Plant, cell & environment.