Seasonal decline in leaf photosynthesis in perennial switchgrass explained by sink limitations and water deficit
Leaf photosynthesis of perennial grasses usually decreases markedly from early to late summer, even when the canopy remains green and environmental conditions are favorable for photosynthesis. Understanding the physiological basis of this photosynthetic decline reveals the potential for yield improv...
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| Published in | Frontiers in plant science Vol. 13; p. 1023571 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Switzerland
Frontiers Research Foundation
04.01.2023
Frontiers Media S.A |
| Subjects | |
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| Abstract | Leaf photosynthesis of perennial grasses usually decreases markedly from early to late summer, even when the canopy remains green and environmental conditions are favorable for photosynthesis. Understanding the physiological basis of this photosynthetic decline reveals the potential for yield improvement. We tested the association of seasonal photosynthetic decline in switchgrass (
Panicum virgatum
L.) with water availability by comparing plants experiencing ambient rainfall with plants in a rainfall exclusion experiment in Michigan, USA. For switchgrass exposed to ambient rainfall, daily net CO
2
assimilation (
A
n
e
t
'
) declined from 0.9 mol CO
2
m
-2
day
-1
in early summer to 0.43 mol CO
2
m
-2
day
-1
in late summer (53% reduction; P<0.0001). Under rainfall exclusion shelters, soil water content was 73% lower and
A
n
e
t
'
was 12% and 26% lower in July and September, respectively, compared to those of the rainfed plants. Despite these differences, the seasonal photosynthetic decline was similar in the season-long rainfall exclusion compared to the rainfed plants;
A
n
e
t
'
in switchgrass under the shelters declined from 0.85 mol CO
2
m
-2
day
-1
in early summer to 0.39 mol CO
2
m
-2
day
-1
(54% reduction; P<0.0001) in late summer. These results suggest that while water deficit limited
A
n
e
t
'
late in the season, abundant late-season rainfalls were not enough to restore
A
n
e
t
'
in the rainfed plants to early-summer values suggesting water deficit was not the sole driver of the decline. Alongside change in photosynthesis, starch in the rhizomes increased 4-fold (P<0.0001) and stabilized when leaf photosynthesis reached constant low values. Additionally, water limitation under shelters had no negative effects on the timing of rhizome starch accumulation, and rhizome starch content increased ~ 6-fold. These results showed that rhizomes also affect leaf photosynthesis during the growing season. Towards the end of the growing season, when vegetative growth is completed and rhizome reserves are filled, diminishing rhizome sink activity likely explained the observed photosynthetic declines in plants under both ambient and reduced water availability. |
|---|---|
| AbstractList | Leaf photosynthesis of perennial grasses usually decreases markedly from early to late summer, even when the canopy remains green and environmental conditions are favorable for photosynthesis. Understanding the physiological basis of this photosynthetic decline reveals the potential for yield improvement. We tested the association of seasonal photosynthetic decline in switchgrass (
Panicum virgatum
L.) with water availability by comparing plants experiencing ambient rainfall with plants in a rainfall exclusion experiment in Michigan, USA. For switchgrass exposed to ambient rainfall, daily net CO
2
assimilation (
A
n
e
t
'
) declined from 0.9 mol CO
2
m
-2
day
-1
in early summer to 0.43 mol CO
2
m
-2
day
-1
in late summer (53% reduction; P<0.0001). Under rainfall exclusion shelters, soil water content was 73% lower and
A
n
e
t
'
was 12% and 26% lower in July and September, respectively, compared to those of the rainfed plants. Despite these differences, the seasonal photosynthetic decline was similar in the season-long rainfall exclusion compared to the rainfed plants;
A
n
e
t
'
in switchgrass under the shelters declined from 0.85 mol CO
2
m
-2
day
-1
in early summer to 0.39 mol CO
2
m
-2
day
-1
(54% reduction; P<0.0001) in late summer. These results suggest that while water deficit limited
A
n
e
t
'
late in the season, abundant late-season rainfalls were not enough to restore
A
n
e
t
'
in the rainfed plants to early-summer values suggesting water deficit was not the sole driver of the decline. Alongside change in photosynthesis, starch in the rhizomes increased 4-fold (P<0.0001) and stabilized when leaf photosynthesis reached constant low values. Additionally, water limitation under shelters had no negative effects on the timing of rhizome starch accumulation, and rhizome starch content increased ~ 6-fold. These results showed that rhizomes also affect leaf photosynthesis during the growing season. Towards the end of the growing season, when vegetative growth is completed and rhizome reserves are filled, diminishing rhizome sink activity likely explained the observed photosynthetic declines in plants under both ambient and reduced water availability. Leaf photosynthesis of perennial grasses usually decreases markedly from early to late summer, even when the canopy remains green and environmental conditions are favorable for photosynthesis. Understanding the physiological basis of this photosynthetic decline reveals the potential for yield improvement. We tested the association of seasonal photosynthetic decline in switchgrass (Panicum virgatum L.) with water availability by comparing plants experiencing ambient rainfall with plants in a rainfall exclusion experiment in Michigan, USA. For switchgrass exposed to ambient rainfall, daily net CO2 assimilation ( A n e t ' ) declined from 0.9 mol CO2 m-2 day-1 in early summer to 0.43 mol CO2 m-2 day-1 in late summer (53% reduction; P<0.0001). Under rainfall exclusion shelters, soil water content was 73% lower and A n e t ' was 12% and 26% lower in July and September, respectively, compared to those of the rainfed plants. Despite these differences, the seasonal photosynthetic decline was similar in the season-long rainfall exclusion compared to the rainfed plants; A n e t ' in switchgrass under the shelters declined from 0.85 mol CO2 m-2 day-1 in early summer to 0.39 mol CO2 m-2 day-1 (54% reduction; P<0.0001) in late summer. These results suggest that while water deficit limited A n e t ' late in the season, abundant late-season rainfalls were not enough to restore A n e t ' in the rainfed plants to early-summer values suggesting water deficit was not the sole driver of the decline. Alongside change in photosynthesis, starch in the rhizomes increased 4-fold (P<0.0001) and stabilized when leaf photosynthesis reached constant low values. Additionally, water limitation under shelters had no negative effects on the timing of rhizome starch accumulation, and rhizome starch content increased ~ 6-fold. These results showed that rhizomes also affect leaf photosynthesis during the growing season. Towards the end of the growing season, when vegetative growth is completed and rhizome reserves are filled, diminishing rhizome sink activity likely explained the observed photosynthetic declines in plants under both ambient and reduced water availability.Leaf photosynthesis of perennial grasses usually decreases markedly from early to late summer, even when the canopy remains green and environmental conditions are favorable for photosynthesis. Understanding the physiological basis of this photosynthetic decline reveals the potential for yield improvement. We tested the association of seasonal photosynthetic decline in switchgrass (Panicum virgatum L.) with water availability by comparing plants experiencing ambient rainfall with plants in a rainfall exclusion experiment in Michigan, USA. For switchgrass exposed to ambient rainfall, daily net CO2 assimilation ( A n e t ' ) declined from 0.9 mol CO2 m-2 day-1 in early summer to 0.43 mol CO2 m-2 day-1 in late summer (53% reduction; P<0.0001). Under rainfall exclusion shelters, soil water content was 73% lower and A n e t ' was 12% and 26% lower in July and September, respectively, compared to those of the rainfed plants. Despite these differences, the seasonal photosynthetic decline was similar in the season-long rainfall exclusion compared to the rainfed plants; A n e t ' in switchgrass under the shelters declined from 0.85 mol CO2 m-2 day-1 in early summer to 0.39 mol CO2 m-2 day-1 (54% reduction; P<0.0001) in late summer. These results suggest that while water deficit limited A n e t ' late in the season, abundant late-season rainfalls were not enough to restore A n e t ' in the rainfed plants to early-summer values suggesting water deficit was not the sole driver of the decline. Alongside change in photosynthesis, starch in the rhizomes increased 4-fold (P<0.0001) and stabilized when leaf photosynthesis reached constant low values. Additionally, water limitation under shelters had no negative effects on the timing of rhizome starch accumulation, and rhizome starch content increased ~ 6-fold. These results showed that rhizomes also affect leaf photosynthesis during the growing season. Towards the end of the growing season, when vegetative growth is completed and rhizome reserves are filled, diminishing rhizome sink activity likely explained the observed photosynthetic declines in plants under both ambient and reduced water availability. Leaf photosynthesis of perennial grasses usually decreases markedly from early to late summer, even when the canopy remains green and environmental conditions are favorable for photosynthesis. Understanding the physiological basis of this photosynthetic decline reveals the potential for yield improvement. We tested the association of seasonal photosynthetic decline in switchgrass (Panicum virgatum L.) with water availability by comparing plants experiencing ambient rainfall with plants in a rainfall exclusion experiment in Michigan, USA. For switchgrass exposed to ambient rainfall, daily net CO2 assimilation ( Anet') declined from 0.9 mol CO2 m-2 day-1 in early summer to 0.43 mol CO2 m-2 day-1 in late summer (53% reduction; P<0.0001). Under rainfall exclusion shelters, soil water content was 73% lower and Anet' was 12% and 26% lower in July and September, respectively, compared to those of the rainfed plants. Despite these differences, the seasonal photosynthetic decline was similar in the season-long rainfall exclusion compared to the rainfed plants; Anet' in switchgrass under the shelters declined from 0.85 mol CO2 m-2 day-1 in early summer to 0.39 mol CO2 m-2 day-1 (54% reduction; P<0.0001) in late summer. These results suggest that while water deficit limited Anet' late in the season, abundant late-season rainfalls were not enough to restore Anet' in the rainfed plants to early-summer values suggesting water deficit was not the sole driver of the decline. Alongside change in photosynthesis, starch in the rhizomes increased 4-fold (P<0.0001) and stabilized when leaf photosynthesis reached constant low values. Additionally, water limitation under shelters had no negative effects on the timing of rhizome starch accumulation, and rhizome starch content increased ~ 6-fold. These results showed that rhizomes also affect leaf photosynthesis during the growing season. Towards the end of the growing season, when vegetative growth is completed and rhizome reserves are filled, diminishing rhizome sink activity likely explained the observed photosynthetic declines in plants under both ambient and reduced water availability. Leaf photosynthesis of perennial grasses usually decreases markedly from early to late summer, even when the canopy remains green and environmental conditions are favorable for photosynthesis. Understanding the physiological basis of this photosynthetic decline reveals the potential for yield improvement. We tested the association of seasonal photosynthetic decline in switchgrass ( L.) with water availability by comparing plants experiencing ambient rainfall with plants in a rainfall exclusion experiment in Michigan, USA. For switchgrass exposed to ambient rainfall, daily net CO assimilation ( ) declined from 0.9 mol CO m day in early summer to 0.43 mol CO m day in late summer (53% reduction; P<0.0001). Under rainfall exclusion shelters, soil water content was 73% lower and was 12% and 26% lower in July and September, respectively, compared to those of the rainfed plants. Despite these differences, the seasonal photosynthetic decline was similar in the season-long rainfall exclusion compared to the rainfed plants; in switchgrass under the shelters declined from 0.85 mol CO m day in early summer to 0.39 mol CO m day (54% reduction; P<0.0001) in late summer. These results suggest that while water deficit limited late in the season, abundant late-season rainfalls were not enough to restore in the rainfed plants to early-summer values suggesting water deficit was not the sole driver of the decline. Alongside change in photosynthesis, starch in the rhizomes increased 4-fold (P<0.0001) and stabilized when leaf photosynthesis reached constant low values. Additionally, water limitation under shelters had no negative effects on the timing of rhizome starch accumulation, and rhizome starch content increased ~ 6-fold. These results showed that rhizomes also affect leaf photosynthesis during the growing season. Towards the end of the growing season, when vegetative growth is completed and rhizome reserves are filled, diminishing rhizome sink activity likely explained the observed photosynthetic declines in plants under both ambient and reduced water availability. Leaf photosynthesis of perennial grasses usually decreases markedly from early to late summer, even when the canopy remains green and environmental conditions are favorable for photosynthesis. Understanding the physiological basis of this photosynthetic decline reveals the potential for yield improvement. We tested the association of seasonal photosynthetic decline in switchgrass (Panicum virgatum L.) with water availability by comparing plants experiencing ambient rainfall with plants in a rainfall exclusion experiment in Michigan, USA. For switchgrass exposed to ambient rainfall, daily net CO2 assimilation ( A'net) declined from 0.9 mol CO2 m-2 day-1 in early summer to 0.43 mol CO2 m-2 day-1 in late summer (53% reduction; P<0.0001). Under rainfall exclusion shelters, soil water content was 73% lower and A'net was 12% and 26% lower in July and September, respectively, compared to those of the rainfed plants. Despite these differences, the seasonal photosynthetic decline was similar in the season-long rainfall exclusion compared to the rainfed plants; A'net in switchgrass under the shelters declined from 0.85 mol CO2 m-2 day-1 in early summer to 0.39 mol CO2 m-2 day-1 (54% reduction; P<0.0001) in late summer. These results suggest that while water deficit limited A'net late in the season, abundant late-season rainfalls were not enough to restore A'net in the rainfed plants to early-summer values suggesting water deficit was not the sole driver of the decline. Alongside change in photosynthesis, starch in the rhizomes increased 4-fold (P<0.0001) and stabilized when leaf photosynthesis reached constant low values. Additionally, water limitation under shelters had no negative effects on the timing of rhizome starch accumulation, and rhizome starch content increased ~6-fold. These results showed that rhizomes also affect leaf photosynthesis during the growing season. Towards the end of the growing season, when vegetative growth is completed and rhizome reserves are filled, diminishing rhizome sink activity likely explained the observed photosynthetic declines in plants under both ambient and reduced water availability. |
| Author | Robertson, G. Philip Abraha, Michael Walker, Berkley James Hamilton, Stephen K. Tejera-Nieves, Mauricio Chen, Jiquan |
| AuthorAffiliation | 2 Great Lakes Bioenergy Research Center, Michigan State University , East Lansing, MI , United States 8 Department of Plant Biology, Michigan State University , East Lansing, MI , United States 4 Center for Global Change and Earth Observations, Michigan State University , East Lansing, MI , United States 5 Department of Geography, Environment, and Spatial Sciences, Michigan State University , East Lansing, MI , United States 6 Department of Integrative Biology, Michigan State University , East Lansing, MI , United States 1 MSU-DOE Plant Research Laboratory, Michigan State University , East Lansing, MI , United States 7 Department of Plant, Soil, and Microbial Sciences, Michigan State University , East Lansing, MI , United States 3 W. K. Kellogg Biological Station, Michigan State University , Hickory Corners, MI , United States |
| AuthorAffiliation_xml | – name: 8 Department of Plant Biology, Michigan State University , East Lansing, MI , United States – name: 6 Department of Integrative Biology, Michigan State University , East Lansing, MI , United States – name: 3 W. K. Kellogg Biological Station, Michigan State University , Hickory Corners, MI , United States – name: 5 Department of Geography, Environment, and Spatial Sciences, Michigan State University , East Lansing, MI , United States – name: 4 Center for Global Change and Earth Observations, Michigan State University , East Lansing, MI , United States – name: 1 MSU-DOE Plant Research Laboratory, Michigan State University , East Lansing, MI , United States – name: 2 Great Lakes Bioenergy Research Center, Michigan State University , East Lansing, MI , United States – name: 7 Department of Plant, Soil, and Microbial Sciences, Michigan State University , East Lansing, MI , United States |
| Author_xml | – sequence: 1 givenname: Mauricio surname: Tejera-Nieves fullname: Tejera-Nieves, Mauricio – sequence: 2 givenname: Michael surname: Abraha fullname: Abraha, Michael – sequence: 3 givenname: Jiquan surname: Chen fullname: Chen, Jiquan – sequence: 4 givenname: Stephen K. surname: Hamilton fullname: Hamilton, Stephen K. – sequence: 5 givenname: G. Philip surname: Robertson fullname: Robertson, G. Philip – sequence: 6 givenname: Berkley James surname: Walker fullname: Walker, Berkley James |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36684783$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1922709$$D View this record in Osti.gov |
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| Cites_doi | 10.1016/j.plaphy.2016.04.020 10.1371/journal.pone.0192555 10.1093/jxb/erq144 10.1111/jac.12336 10.1093/JXB/ERX241 10.1371/journal.pone.0222080 10.1007/s11099-015-0108-3 10.1086/505797 10.1016/j.tplants.2019.04.005 10.1007/s00425-015-2436-8 10.1016/j.njas.2016.03.011 10.1080/07352680500316433 10.1111/pce.13512 10.1093/jxb/erv129 10.1016/J.JPLPH.2008.01.008 10.1007/s12155-017-9879-7 10.1104/pp.16.00545 10.1007/S12155-009-9055-9 10.3389/fenrg.2018.00054 10.1093/treephys/26.9.1173 10.1007/s10142-014-0393-0 10.1111/j.1365-3040.2007.01708.x 10.3389/FPLS.2016.00822 10.1007/s12155-016-9768-5 10.1111/ppl.12331 10.1111/gcbb.12745 10.3390/plants9101266 10.1007/s12155-022-10408-2 10.1111/j.1469-8137.2006.01785.x 10.1016/j.plaphy.2004.12.009 10.1186/s13068-020-01810-z 10.1007/s13595-020-00940-6 10.1016/J.AGRFORMET.2018.02.016 10.1007/S12155-009-9074-6 10.1111/gcbb.12118 10.1186/s13068-015-0342-8 10.1111/J.1399-3054.1997.TB01059.X 10.1071/CP11128 10.2135/CROPSCI2006.04.0260 10.3390/AGRONOMY10070940 10.1016/j.envpol.2019.06.062 10.1016/j.agrformet.2012.11.006 10.1071/FP17268 10.1007/s00484-012-0614-y 10.1016/j.envexpbot.2018.10.016 10.1016/j.plantsci.2009.09.003 10.1007/s00468-015-1290-4 10.1007/s12155-012-9287-y 10.1093/jxb/ern310 10.1111/J.1365-2486.2005.001002.X 10.3389/fpls.2013.00272 10.1007/s11284-015-1330-y 10.1016/j.agee.2015.10.018 10.3389/fpls.2021.643143 10.5194/BG-15-5015-2018 10.1093/jxb/erac382 10.18637/jss.v067.i01 10.1007/s12155-019-10066-x 10.1002/ajb2.1612 10.1093/jxb/eraa459 10.1111/j.1438-8677.2008.00086.x |
| ContentType | Journal Article |
| Copyright | Copyright © 2023 Tejera-Nieves, Abraha, Chen, Hamilton, Robertson and Walker James. Copyright © 2023 Tejera-Nieves, Abraha, Chen, Hamilton, Robertson and Walker James 2023 Tejera-Nieves, Abraha, Chen, Hamilton, Robertson and Walker James |
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| Keywords | sink limitation circadian perennial grass source- sink- relationships drought storage carbohydrates C4 photosynthesis photosyhthesis |
| Language | English |
| License | Copyright © 2023 Tejera-Nieves, Abraha, Chen, Hamilton, Robertson and Walker James. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 SC0018409 USDOE Office of Science (SC), Biological and Environmental Research (BER) Reviewed by: Bin Xu, Nanjing Agricultural University, China; Wangfeng Zhang, Shihezi University, China Edited by: Jiban Shrestha, Nepal Agricultural Research Council, Nepal This article was submitted to Plant Abiotic Stress, a section of the journal Frontiers in Plant Science |
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| Title | Seasonal decline in leaf photosynthesis in perennial switchgrass explained by sink limitations and water deficit |
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