Abstract
Low light conditions not only induce leaf senescence, but also photosynthetic acclimation. This study aimed to determine whether plants exhibit photosynthetic acclimation during low-light-induced leaf senescence. The influences of shading on leaf senescence and photosynthetic acclimation were explored in post-anthesis maize plants. The results showed that whole shading (WS) of maize plants accelerated leaf senescence, whereas partial shading (PS) slowed leaf senescence. WS led to larger decreases in the photosynthetic rate (Pn) and stomatal conductance (Gs) compared to those of the PS treatment. Interestingly, chlorophyll a fluorescence (ChlF) demonstrated that the absorption flux (ABS/CSo) and trapped energy flux (TRo/CSo) per cross section in leaves remained relatively stable under WS, whereas significant decreases in the active PSII reaction centers (RC/CSo) resulted in considerable increases in absorption (ABS/RC) and trapped energy flux (TRo/RC) per reaction center. ABS/CSo, TRo/CSo, ABS/RC, and TRo/RC increased markedly under PS, whereas there were slight decreases in RC/CSo and electron transport activity. These results suggest that the PS treatment resulted in obvious improvements in the absorption and capture of light energy in shaded leaves. Further analysis demonstrated that both the WS and PS treatments resulted in a greater decrease in the activity of Rubisco compared to that of phosphoenolpyruvate carboxylase (PEPC). Moreover, PEPC activity in PS was maintained at a high level. Consequently, the current study proposed that the improvement of the absorption and capture of light energy and the maintenance of PEPC activity of mesophyll cells were due to photosynthetic acclimation of low-light-induced leaf senescence in maize plants. In addition, the rate of senescence of vascular bundle cells in maize leaves exceeded that of mesophyll cells under low light, showing obvious tissue specificity.
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Abbreviations
- ABS/CSo :
-
Absorption flux per cross section
- ABS/RC:
-
Absorption flux per reaction center
- ChlF:
-
Chlorophyll a fluorescence
- Ci :
-
Intercellular carbon dioxide concentration
- ETo/CSo :
-
Electron transport flux per cross section
- ETo/RC:
-
Electron transport flux per reaction center (at t = 0)
- Gs :
-
Stomatal conductance
- MDA:
-
Malondialdehyde
- PEPC:
-
Phosphoenolpyruvate carboxylase
- Pn :
-
Net photosynthetic rate
- PS:
-
Partial shading
- RC/CSo :
-
Density of reaction centers
- TRo/CSo :
-
Trapped energy flux per cross section
- TRo/RC:
-
Trapped energy flux per reaction center (at t = 0)
- WS:
-
Whole shading
- Ѱo:
-
Probability that a trapped exciton moves an electron into the electron transport chain beyond Q–A
- φEo :
-
The quantum yield of electron transport beyond QA
- φpo :
-
The maximum quantum yield of primary photochemistry
References
Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–5. https://doi.org/10.1104/pp.24.1.1
Bi HG, Liu PP, Jiang ZG, Ai XZ (2017) Overexpression of the rubisco activase gene improves growth and low temperature and weak light tolerance in Cucumis sativus. Physiol Plant 161:224–234. https://doi.org/10.1111/ppl.12587
Briggs WR, Christie JM (2002) Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204–210. https://doi.org/10.1016/S1360-1385(02)02245-8
Brouwer B, Ziolkowska A, Bagard M, Keech O, Gardeström P (2012) The impact of light intensity on shade-induced leaf senescence. Plant Cell Environ 35:1084–1098. https://doi.org/10.1111/j.1365-3040.2011.02474.x
Brouwer B, Gardeström P, Keech O (2014) In response to partial plant shading, the lack of phytochrome A does not directly induce leaf senescence but alters the fine-tuning of chlorophyll biosynthesis. J Exp Bot 65:4037–4049. https://doi.org/10.1093/jxb/eru060
Evans JR (1999) Leaf anatomy enables more equal access to light and CO2 between chloroplasts. New Phytol 143:93–104. https://doi.org/10.1046/j.1469-8137.1999.00440.x
Evans JR, Vogelmann TC (2006) Photosynthesis within isobilateral Eucalyptus pauciflora leaves. New Phytol 171:771–782. https://doi.org/10.1111/j.1469-8137.2006.01789.x
Fukayama H, Hatch MD, Tamai T, Tsuchida H, Sudoh S, Furbank RT, Miyao M (2003) Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase over-produced in transgenic rice plants. Photosynth Res 77:227–239. https://doi.org/10.1023/A:1025861431886
Garapati P, Xue GP, Munne-Bosch S, Balazadeh S (2015) Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. Plant Physiol 168:1122–1139. https://doi.org/10.1104/pp.15.00567
Ghorbanzadeh P, Aliniaeifard S, Esmaeili M, Mashal M, Azadegan B, Seif M (2020) Dependency of growth, water use efficiency, chlorophyll fluorescence, and stomatal characteristics of lettuce plants to light intensity. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10269-z
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611. https://doi.org/10.1007/s004250050524
Jiang CD, Shi L, Gao HY, Schansker G, Toth SZ, Strasser RJ (2006) Development of photosystems 2 and 1 during leaf growth in grapevine seedlings probed by chlorophyll a fluorescence transient and 820 nm transmission in vivo. Photosynthetica 44(3):454–463. https://doi.org/10.1007/s11099-006-0050-5
Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102. https://doi.org/10.1007/s11738-016-2113-y
Kalaji HM, Rastogi A, Živcak M, Brestic M, Daszkowska-Golec A, Sitko K, Alsharafa KY, Lotfi R, Stypinski P, Samborska IA, Cetner MD (2018) Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica 56(3):953–961. https://doi.org/10.1007/s11099-018-0766-z
Keech O, Pesquet E, Ahad A, Askne A, Nordvall D, Vodnala SM, Tuominen H, Hurry V, Dizengremel P, Gardeström P (2007) The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves. Plant Cell Environ 30:1523–1534. https://doi.org/10.1111/j.1365-3040.2007.01724.x
Kim J, Kim JH, Lyu JI, Woo HR, Lim PO (2018) New insights into the regulation of leaf senescence in Arabidopsis. J Exp Bot 69:787–799. https://doi.org/10.1093/jxb/erx287
Law SR, Chrobok D, Juvany M, Delhomme N, Linden P, Brouwer B, Ahad A, Moritz T, Jansson S, Gardeström P, Keech O (2018) Darkened leaves use different metabolic strategies for senescence and survival. Plant Physiol 177:132–150. https://doi.org/10.1104/pp.18.00062
Li ZZ, Liu DH, Zhao SW, Jiang CD, Shi L (2014) Mechanisms of photoinhibition induced by high light in Hosta grown outdoors. J Plant Ecol 38(7):720–728. https://doi.org/10.3724/SP.J.1258.2014.00067 (in Chinese)
Li J, Xie RZ, Wang KR, Ming B, Guo YQ, Zhang GQ, Li SK (2015) Variations in maize dry matter, harvest index, and grain yield with plant density. Agron J 107:1–6. https://doi.org/10.2134/agronj14.0522
Louis L, Pierre D, Jean-Philippe B (2008) Foliar CO2 fixation in bean (Phaseolus vulgaris L.) submitted to elevated ozone: Distinct changes in Rubisco and PEPc activities in relation to pigment content. Ecotox Environ Safe 69:531–540. https://doi.org/10.1016/j.ecoenv.2006.10.010
Ma JY, Sun W, Koteyeva NK, Voznesenskaya E, Stutz SS, Gandin A, Smith-Moritz AM, Heazlewood JL, Cousins AB (2017) Influence of light and nitrogen on the photosynthetic efficiency in the C4 plant Miscanthus X giganteus. Photosynth Res 131:1–13. https://doi.org/10.1007/s11120-016-0281-7
Maness N (2010) Extraction and analysis of soluble carbohydrates. In: Sunkar R (ed) Plant stress tolerance. Humana Press, Totowa, pp 341–370. https://doi.org/10.1007/978-1-60761-702-0_22
Nishio JN, Sun J, Vogelmann TC (1993) Carbon fixation gradients across spinach leaves do not follow internal light gradients. Plant Cell 5:953–961. https://doi.org/10.1105/tpc.5.8.953
Oda-Yamamizo C, Mitsuda N, Sakamoto S, Ogawa D, Ohme-Takagi M, Ohmiya A (2016) The NAC transcription factor ANAC046 is a positive regulator of chlorophyll degradation and senescence in Arabidopsis leaves. Sci Rep 6:23609. https://doi.org/10.1038/srep23609
Panda D, Sarkar RK (2013) Natural leaf senescence: probed by chlorophyll fluorescence, CO2 photosynthetic rate and antioxidant enzyme activities during grain filling in different rice cultivars. Physiol Mol Biol Plants 19:43–51. https://doi.org/10.1007/s12298-012-0142-6
Porra RJ, Scheer H (2019) Towards a more accurate future for chlorophyll a and b determinations: the inaccuracies of Daniel Arnon’s assay. Photosynth Res 140:215–219. https://doi.org/10.1007/s11120-018-0579-8
Qiao MY, Zhang YJ, Liu LA, Shi L, Ma QH, Jiang CD (2019) Effects of changing frequency of fluctuating light on photosynthesis in cucumber seedlings. Sci Sin Vitae 49:280–288. https://doi.org/10.1360/N052018-00253 (in Chinese)
Sharwood RE, Sonawane BV, Ghannoum O (2014) Photosynthetic flexibility in maize exposed to salinity and shade. J Exp Bot 65:3715–3724. https://doi.org/10.1093/jxb/eru130
Slattery RA, Grennan AK, Sivaguru M, Sozzani R, Ort DR (2016) Light sheet microscopy reveals more gradual light attenuation in light-green versus dark-green soybean leaves. J Exp Bot 67:4697–4709. https://doi.org/10.1093/jxb/erw246
Strasser RJ, Tsimilli-Michael M (2001) Structure function relationship in the photosynthetic apparatus: a biophysical approach. In: Pardha SP (ed) Biophysical processes in living systems. Science Publ, Enfield, pp 271–303
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration. Springer, Dordrecht, pp 321–362
Vogelmann TC, Han T (2000) Measurement of gradients of absorbed light in spinach leaves from chlorophyll fluorescence profiles. Plant Cell Environ 23:1303–1311. https://doi.org/10.1046/j.1365-3040.2000.00649.x
Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886. https://doi.org/10.1104/pp.010312
Weng XY, Xu HX, Jiang DA (2005) Characteristics of gas exchange, chlorophyll fluorescence and expression of key enzymes in photosynthesis during leaf senescence in rice plants. J Integr Plant Biol 47(5):560–566. https://doi.org/10.1111/j.1744-7909.2005.00098.x
Wu HY, Zhang YJ, Zhang WF, Wang KR, Li SK, Jiang CD (2019) Photosynthetic characteristics of senescent leaf induced by high planting density of maize at heading stage in the field. Acta Agron Sin 45(2):248–255. https://doi.org/10.3724/SP.J.1006.2019.83042 (in Chinese)
Wu HY, Dong FQ, Liu LA, Shi L, Zhang WF, Jiang CD (2020) Dorsoventral variation in photosynthesis during leaf senescence probed by chlorophyll a fluorescence induction kinetics in cucumber and maize plants. Photosynthetica 58(SI):479–487. https://doi.org/10.32615/ps.2020.005
Yabiku T, Akamatsu S, Ueno S (2020) Light reacclimatization of lower leaves in C4 maize canopies grown at two planting densities. Photosynthetica 58(3):732–739. https://doi.org/10.32615/ps.2020.029
Yang XH, Chen XY, Ge QY, Li B, Tong YP, Zhang AM, Li ZS, Kuang TY, Lu CM (2006) Tolerance of photosynthesis to photoinhibition, high temperature and drought stress in flag leaves of wheat: a comparison between a hybridization line and its parents grown under field conditions. Plant Sci 171:389–397. https://doi.org/10.1016/j.plantsci.2006.04.010
Yang B, Tang J, Yu ZH, Khare T, Srivastav A, Datir S, Kumar V (2019) Light stress responses and prospects for engineering light stress tolerance in crop plants. J Plant Growth Regul 38:1489–1506. https://doi.org/10.1007/s00344-019-09951-8
Ye YX, Wen ZR, Yang H, Lu WP, Lu DL (2020) Effects of post-silking water deficit on the leaf photosynthesis and senescence of waxy maize. J Integr Agr 19(9):2216–2228. https://doi.org/10.1016/S2095-3119(20)63158-6
Zeng FL, Wang GJ, Liang YP, Guo NH, Zhu L, Wang Q, Chen HW, Ma DR, Wang JY (2020) Disentangling the photosynthesis performance in japonica rice during natural leaf senescence using OJIP fluorescence transient analysis. Funct Plant Biol 48(2):206–217. https://doi.org/10.1071/FP20104
Zhang YQ, Liu ZJ, Chen YD, He JX, Bi YR (2015) Phytochrome-interacting factor 5 (PIF5) positively regulates dark-induced senescence and chlorophyll degradation in Arabidopsis. Plant Sci 237:57–68. https://doi.org/10.1016/j.plantsci.2015.05.010
Zivcak M, Brestic M, Kalaji HM, Govindjee (2014) Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynth Res 119:339–354. https://doi.org/10.1007/s11120-014-9969-8
Acknowledgements
This study was supported by the National Natural Science Foundation of China (31571576 and 31970350).
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Wu, HY., Liu, LA., Shi, L. et al. Photosynthetic acclimation during low-light-induced leaf senescence in post-anthesis maize plants. Photosynth Res 150, 313–326 (2021). https://doi.org/10.1007/s11120-021-00851-1
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DOI: https://doi.org/10.1007/s11120-021-00851-1