Ethylene production under high temperature stress causes premature leaf senescence in soybean
Maduraimuthu Djanaguiraman A and P. V. Vara Prasad A BA Department of Agronomy, 2004 Throckmorton Plant Science Center, Kansas State University, Manhattan, 66506 KS, USA.
B Corresponding author. Email: vara@ksu.edu
Functional Plant Biology 37(11) 1071-1084 https://doi.org/10.1071/FP10089
Submitted: 19 April 2010 Accepted: 31 July 2010 Published: 22 October 2010
Abstract
Leaf senescence in soybean (Glycine max L. Merr.) occurs during the later stages of reproductive development and can be triggered or enhanced by high temperature (HT) stress. Ethylene production can trigger premature leaf senescence, but it is unclear whether HT stress produces ethylene and the subsequent influence on physiology and yield of soybean is also uncertain. We hypothesised that ethylene produced under HT stress is involved in premature leaf senescence and that use of an ethylene perception inhibitor would influence physiology and yield. Objectives of this study were to (1) quantify HT-stress-induced ethylene production; (2) quantify effects of HT stress and application of an ethylene perception inhibitor (1-methylcyclopropene; 1-MCP) on source strength traits such as photosynthetic rate, oxidant production, membrane damage and sugar accumulation; and (3) evaluate efficacy of 1-MCP on minimising HT-stress-induced effects on physiological and yield traits. Soybean plants were exposed to HT (38/28°C) or optimum temperature (OT, 28/18°C) for 14 days at the beginning of pod set. Plants at each temperature were treated with 1 μg L–1 1-MCP or left untreated (control). HT stress enhanced ethylene production rates in leaves and pods by 3.2- and 2.1-fold over OT. HT stress decreased photochemical efficiency (5.8%), photosynthetic rate (12.7%), sucrose content (21.5%), superoxide dismutase (13.3%), catalase (44.6%) and peroxidase (42.9%) enzymes activity and increased superoxide radical (63%) and hydrogen peroxide (70.4%) content and membrane damage (54.7%) compared with OT. Application of 1-MCP decreased ethylene production rate and premature leaf senescence traits by enhancing the antioxidant defence system. HT stress decreased seed set percentage (18.6%), seed size (64.5%) and seed yield plant–1 (71.4%) compared with OT, however, foliar spray of 1-MCP increased the seed set percent and seed size, which resulted in a higher yield than the unsprayed control. The present study showed HT stress increased ethylene production rate, which triggered premature leaf senescence, whereas 1-MCP application reduced or postponed premature leaf senescence traits by inhibiting ethylene production.
Additional keywords: antioxidant enzymes, membrane damage, 1-methyl cyclopropene.
Acknowledgements
We thank AgroFresh Inc. for partial financial support. Mention of trademark or proprietary product does not constitute a guarantee or warranty of the product by Kansas State University and does not imply its approval to the exclusion of other products which may also be suitable. Contribution no. 10–274-J from the Kansas Agricultural Experiment Station.
Al-Khatib K, Paulsen GM
(1984) Mode of high temperature injury to wheat during grain development. Physiologia Plantarum 61, 363–368.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Antunes MDC, Sfakiotakis EM
(2000) Effect of high temperature stress on ethylene biosynthesis, respiration and ripening of ‘Hayward’ kiwifruit. Postharvest Biology and Technology 20, 251–259.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Behera TH,
Panda SK, Patra HK
(1999) Chromium ion induced lipid peroxidation in developing wheat seedlings: role of growth hormones. Indian Journal of Plant Physiology 4, 236–238.
|
CAS |
Beyer WF, Fridovich I
(1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry 161, 559–566.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bibi AC,
Oosterhuis DM, Gonias ED
(2008) Photosynthesis, quantum yield of photosystem II, and membrane leakage as affected by high temperatures in cotton genotypes. Journal of Cotton Science 12, 150–159.
|
CAS |
Blankenship SM, Dole JM
(2003) 1-Methylcyclopropene: a review. Postharvest Biology and Technology 28, 1–25.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bruening WP, Egli DB
(2000) Leaf starch accumulation and seed set at phloem-isolated nodes in soybean. Field Crops Research 68, 113–120.
| Crossref | GoogleScholarGoogle Scholar |
Calviño PA,
Sadras VO, Andrade FH
(2003) Development, growth and yield of late-sown soybeans in the southern Pampas. European Journal of Agronomy 19, 265–275.
| Crossref | GoogleScholarGoogle Scholar |
Chaitanya KSK, Naithani SC
(1994) Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn.f. New Phytologist 126, 623–627.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Chamnongpol S,
Willekens H,
Moeder W,
Langebartels C,
Sandermann H,
Van Montagu M,
Inze D, Van Camp W
(1998) Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco. Proceedings of the National Academy of Sciences of the United States of America 95, 5818–5823.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Click RE,
Schlagnhaufer CD,
Arteca RN, Pell EJ
(1995) Ozone induced ethylene emission accelerates the loss of ribulose-l,5-bisphosphate carboxylase/oxygenase and nuclear encoded mRNAs in senescing potato leaves. Plant Physiology 109, 891–898.
| PubMed |
Crafts-Brandner SJ, Salvucci ME
(2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proceedings of the National Academy of Sciences of the United States of America 97, 13 430–13 435.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Desikan R,
Cheung MK,
Clarke A,
Golding S,
Sagi M,
Fluhr R,
Rock C,
Hancock J, Neill S
(2004) Hydrogen peroxide is a common signal for darkness and ABA-induced stomatal closure in Pisum sativum. Functional Plant Biology 31, 913–920.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Desikan R,
Last K,
Harrett-Williams R,
Tagliavia C,
Harter K,
Hooley R,
Hancock JT, Neill SJ
(2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. The Plant Journal 47, 907–916.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Dias AS,
Barreiro MG,
Campos PS,
Ramalho JC, Lidon FC
(2010) Wheat cellular membrane thermotolerance under heat stress. Journal of Agronomy and Crop Science 196, 100–108.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Diaz C,
Purdy S,
Christ A,
Morot-Gaudry JF,
Wingler A, Masclaux-Daubresse C
(2005) Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis thaliana: a metabolic profiling approach. Plant Physiology 138, 898–908.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Djanaguiraman M,
Annie Sheeba J,
Durga Devi D, Bangarusamy U
(2009) Cotton leaf senescence can be delayed by nitrophenolate spray through enhanced antioxidant defense system. Journal Agronomy & Crop Science 195, 213–224.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gallardo M,
Delgado MM,
Sanchez-Calle IM, Matilla AJ
(1991) Ethylene production and 1-aminocyclopropane-1-carboxylic acid conjugation in thermoinhibited Cicer arietinum L. seeds. Plant Physiology 97, 122–127.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Geigenberger P,
Geiger M, Stitt M
(1998) High-temperature perturbation of starch synthesis is attributable to inhibition of ADP-glucose pyrophosphorylase by decreased levels of glycerate-3-phosphate in growing potato tubers. Plant Physiology 117, 1307–1316.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gibson LR, Mullen RE
(1996) Influence of day and night temperature on soybean seed yield. Crop Science 36, 98–104.
| Crossref | GoogleScholarGoogle Scholar |
Gossauer A, Engel N
(1996) Chlorophyll catabolism – structures, mechanisms, conversions. Journal of Photochemistry and Photobiology. B, Biology 32, 141–151.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Grbic V, Bleecker A
(1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. The Plant Journal 8, 595–602.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Grove S,
Sabat C, Mohanty P
(1986) Effect of temperature on photosynthetic activities of senescent detached wheat leaves. Plant & Cell Physiology 27, 117–126.
Gunderson CA, Taylor GE
(1991) Ethylene directly inhibits foliar gas exchange in Glycine max. Plant Physiology 95, 337–339.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hays DB,
Do JH,
Mason RE,
Morgan G, Scott AF
(2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Science 172, 1113–1123.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
John I,
Drake R,
Farell A,
Cooper W,
Lee P,
Horton P, Grierson D
(1995) Delayed leaf senescence in ethylene-deficient ACC oxidase antisense tomato plants: molecular and physiological analysis. The Plant Journal 7, 483–490.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Jongebloed U,
Szederkenyi J,
Hartig K,
Schobert C, Komor E
(2004) Sequence of morphological and physiological events during natural ageing of a castor bean leaf: sieve tube occlusions and carbohydrate back-up precede chlorophyll degradation. Physiologia Plantarum 120, 338–346.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kawakami EM,
Oosterhuis DM, Snider JL
(2010) Physiological effects of 1-methylcyclo propene on well-watered and water-stressed cotton plants. Journal of Plant Growth Regulation 29, 280–288.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Knudson LL,
Tibbitts TW, Edwards GE
(1977) Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiology 60, 606–608.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Larrigaudière C,
Vilaplana R,
Soria Y, Recasens I
(2004) Oxidative behaviour of Blanquilla pears treated with 1-methylcyclopropene during cold storage. Journal of the Science of Food and Agriculture 84, 1871–1877.
| Crossref | GoogleScholarGoogle Scholar |
Lee S,
Choi H,
Suh S,
Doo IS,
Oh KY,
Choi EJ,
Taylor ATS,
Low PS, Lee Y
(1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiology 121, 147–152.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Li C, Wang G
(2004) Interactions between reactive oxygen species, ethylene and polyamines in leaves of Glycyrrhiza inflata seedlings under root osmotic stress. Plant Growth Regulation 42, 55–60.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Lin CC, Kao CH
(1999) NaCl induced changes in ionically bounds peroxidase activity in roots of rice seedlings. Plant and Soil 216, 147–153.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Liu X, Huang B
(2000) Heat stress injury in relation to membrane lipid peroxidation in creeping bentgrass. Crop Science 40, 503–510.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Lowry OH,
Rosebrough NJ,
Farr AL, Randall RJ
(1951) Protein measurement with the folin phenol reagent. The Journal of Biological Chemistry 193, 265–275.
|
CAS |
PubMed |
Luo Z,
Xu X,
Cai Z, Yan B
(2007) Effects of ethylene and 1-methylcyclopropene (1-MCP) on lignification of postharvest bamboo shoot. Food Chemistry 105, 521–527.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McAinsh MR,
Clayton H,
Mansfield TA, Hetherington AM
(1996) Changes in stomatal behaviour and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiology 111, 1031–1042.
|
CAS |
PubMed |
Miller GL
(1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry 31, 426–428.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Moeder W,
Barry CS,
Tauriainen AA,
Betz C,
Tuomainen J,
Utriainen M,
Grierson D,
Sandermann H,
Langebartels C, Kangasjarvi J
(2002) Ethylene synthesis regulated by bi-phasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclo propane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiology 130, 1918–1926.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Morgan PW,
He CJ, Drew MC
(1992) Intact leaves exhibit a climacteric-like rise in ethylene production before abscission. Plant Physiology 100, 1587–1590.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Morison JIL, Lawlor DW
(1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant, Cell & Environment 22, 659–682.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Munné-Bosch S, Alegre L
(2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Functional Plant Biology 31, 203–216.
| Crossref | GoogleScholarGoogle Scholar |
Munné-Bosch S, Peñuelas J
(2003) Photo- and antioxidative protection during summer leaf senescence in Pistacia lentiscus L. grown under Mediterranean field conditions. Annals of Botany 92, 385–391.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Noctor G, Foyer CH
(1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nooden LD,
Guiamet JJ, John I
(1997) Senescence mechanisms. Physiologia Plantarum 101, 746–753.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Oh SA,
Park JH,
Lee GI,
Paek KH,
Park SK, Nam HG
(1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. The Plant Journal 12, 527–535.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Patterson BD,
Macrae EA, Ferguson IB
(1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Analytical Biochemistry 139, 487–492.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Paul MJ, Pellny TK
(2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Pei ZM,
Murata Y,
Benning G,
Thomine S,
Klusener B,
Allen GJ,
Grill E, Schroeder JI
(2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406, 731–734.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Peiser GD, Yang SF
(1978) Chlorophyll destruction in the presence of bisulfite and linoleic acid hydroperoxides. Phytochemistry 17, 79–84.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Pourtau N,
Mares M,
Purdy S,
Quentin N,
Ruel A, Wingler A
(2006) Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence. Planta 219, 765–772.
Prasad PVV,
Boote KJ, Allen LH
(2006a) Adverse high temperature effects on pollen viability, seed-set, seed yield, and harvest index of grain-sorghum (Sorghum bicolor (L.) Moench) are more severe at elevated carbon dioxide due to higher tissue temperatures. Agricultural and Forest Meteorology 139, 237–251.
| Crossref | GoogleScholarGoogle Scholar |
Prasad PVV,
Boote KJ,
Allen LH, Sheehy JE
(2006b) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Research 95, 398–411.
| Crossref | GoogleScholarGoogle Scholar |
Prasad PVV,
Pisipati SR,
Mutava RN, Tuinstra MR
(2008a) Sensitivity of grain sorghum to high temperature stress during reproductive development. Crop Science 48, 1911–1917.
| Crossref | GoogleScholarGoogle Scholar |
Prasad PVV,
Pisipati SR,
Ristic Z,
Bukovnik U, Fritz A
(2008b) Impact of night-time temperature on physiology and growth of spring wheat. Crop Science 48, 2372–2380.
| Crossref | GoogleScholarGoogle Scholar |
Quirino BF,
Reiter WD, Amasino RM
(2001) One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Molecular Biology 46, 447–457.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ristic Z,
Bukovnik U, Prasad PVV
(2007) Correlation between heat stability of thylakoid membranes and loss of chlorophyll in winter wheat under heat stress. Crop Science 47, 2067–2073.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ristic Z,
Bukovnik U,
Momcilovi I,
Fu J, Prasad PVV
(2008a) Heat induced accumulation of chloroplast protein synthesis elongation factor, EF-Tu, in winter wheat. Journal of Plant Physiology 165, 192–202.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ristic Z,
Bukovnik U,
Prasad PVV, West M
(2008b) A model for prediction of heat stability of photosynthetic membranes. Crop Science 48, 1513–1522.
| Crossref | GoogleScholarGoogle Scholar |
Sairam RK,
Deshmukh PS, Shukla DS
(1997) Tolerance to drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. Journal Agronomy & Crop Science 178, 171–178.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sairam RK,
Srivastava GC, Saxena DC
(2000) Increased antioxidant activity under elevated temperature: a mechanism of heat stress tolerance in wheat genotypes. Biologia Plantarum 43, 245–251.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Samantary S
(2002) Biochemical responses of Cr-tolerant and Cr-sensitive mung bean cultivars grown on varying levels of chromium. Chemosphere 47, 1065–1072.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Scandalios JG
(1993) Oxygen stress and superoxide dismutases. Plant Physiology 101, 7–12.
|
CAS |
PubMed |
Shah NH, Paulsen GM
(2003) Interaction of drought and high temperature on photosynthesis and grain filling in wheat. Plant and Soil 257, 219–226.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sisler EC, Serek M
(1997) Inhibitors of ethylene responses in plants at the receptor level: recent developments. Physiologia Plantarum 100, 577–582.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Smart CM
(1994) Gene expression during leaf senescence. New Phytologist 126, 419–448.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Snider JL,
Oosterhuis DM, Kawakami EM
(2010) Genotypic differences in thermotolerance are dependent upon prestress capacity for antioxidant protection of the photosynthetic apparatus in Gossypium hirsutum. Physiologia Plantarum 138, 268–277.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Stessman D,
Miller A,
Spalding M, Rodermel S
(2002) Regulation of photosynthesis during Arabidopsis leaf development in continuous light. Photosynthesis Research 72, 27–37.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Takeda T,
Yokota A, Shigeoka S
(1995) Resistance of photosynthesis to hydrogen peroxide in algae. Plant & Cell Physiology 36, 1089–1095.
|
CAS |
Tewari AK, Tripathy BC
(1998) Temperature-stress induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiology 117, 851–858.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Thomas H,
Ougham HJ,
Wagstaff C, Stead AD
(2003) Defining senescence and death. Journal of Experimental Botany 54, 1127–1132.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wingler A, Roitsch T
(2008) Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. Plant Biology 10, 50–62.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yang J,
Zhang J,
Wang Z,
Liu K, Wang P
(2006) Post-anthesis development of inferior and superior spikelets in rice in relation to abscissic acid and ethylene. Journal of Experimental Botany 57, 149–160.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yang TF,
Gonzalez-Carranza ZH,
Maunders MJ, Roberts JA
(2008) Ethylene and the regulation of senescence processes in transgenic Nicotiana sylvestris plants. Annals of Botany 101, 301–310.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zacarias L, Reid MS
(1990) Role of growth regulators in the senescence of Arabidopsis thaliana leaves. Physiologia Plantarum 80, 549–554.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Zhang X,
Zhang L,
Dong F,
Gao J,
Galbraith DW, Song CP
(2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiology 126, 1438–1448.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhang CJ,
Chen GX,
Gao XX, Chu CJ
(2006) Photosynthetic decline in flag leaves of two field grown spring wheat cultivars with different senescence properties. South African Journal of Botany 72, 15–23.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
