Abstract
Shading and drought stresses during the flowering stage of maize (Zea mays L.) production cause seed losses, making them two of the major limitations to yield output. The mechanisms by which the two stresses reduce seed numbers are still unclear. Here, different durations of shading and different degrees of drought were applied, accompanied by synchronous pollination, and the early development of fertilized apical kernels was suppressed, with decreases in sucrose and hexose levels and the promotion of ethylene emission. Consequently, the two distinct stresses led to a common consequence: up to 20–30% of the fertilized kernels were aborted at maturity, which accounted for the yield losses under both scenarios. Notably, by removing the shading net or the preventing pollination of the basal kernels, the apical kernels, were partial or fully restored from abortion, with an increased sugar status and suppressed ethylene emission, even under stress conditions. We found that dry matter accumulation within the early stage was positively correlated with sucrose and hexose contents but negatively correlated with ethylene emission. By altering the sugar status within developing kernels, we verified the antagonistic relationships between endogenous ethylene emission and soluble sugars, including sucrose and hexoses. Collectively, these findings suggest that the equilibrium between sugars and ethylene may determine the development or abortion of early developing kernels exposed to environmental stresses.
Similar content being viewed by others
References
Andersen MN, Asch F, Wu Y, Jensen CR, Næsted H, Mogensen VO, Koch KE (2002) Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize. Plant Physiol 130:591–604
Cheng CY, Lur HS (1996) Ethylene may be involved in abortion of the maize caryopsis. Physiol Plant 98:245–252
Chincinska IA, Liesche J, Krugel U, Michalska J, Geigenberger P, Grimm B, Kuhn C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146:515–528
Feng H-Y, Wang Z-M, Kong F-N, Zhang M-J, Zhou S-L (2011) Roles of carbohydrate supply and ethylene, polyamines in maize kernel set. J Integr Plant Biol 53:388–398
Gao J, Zhao B, Dong S, Liu P, Ren B, Zhang J (2017) Response of summer maize photosynthate accumulation and distribution to shading stress assessed by using 13CO2 stable isotope tracer in the field. Front Plant Sci 8:1821. https://doi.org/10.3389/fpls.2017.01821
Gao Z, Feng H-Y, Liang X-G, Zhang L, Lin S, Zhao X, Shen S, Zhou L-L, Zhou S-L (2018) Limits to maize productivity in the North China Plain: A comparison analysis for spring and summer maize. Field Crops Res 228:39–47
Hanft JM, Jones RJ (1986) Kernel Abortion in Maize I. Carbohydrate concentration patterns and acid invertase activity of maize kernels induced to abort in vitro. Plant Physiol 81:503–510
Hays DB, Do JH, Mason RE, Morgan G, Finlayson SA (2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Sci 172:1113–1123
Hiyane R, Hiyane S, Tang AC, Boyer JS (2010) Sucrose feeding reverses shade-induced kernel losses in maize. Ann Bot 106:395–403
Hong JH, Cowan AK, Lee SK (2004) Glucose inhibits ACC oxidase activity and ethylene biosynthesis in ripening tomato fruit. Plant Growth Regul 43:81–87
Jeannette E, Reyss A, Gregory N, Gantet P, Prioul JL (2000) Carbohydrate metabolism in a heat-girdled maize source leaf. Plant Cell Environ 23:61–69
Mclaughlin JE, Boyer JS (2004) Glucose localization in maize ovaries when kernel number decreases at low water potential and sucrose is fed to the stems. Ann Bot 94:75–86
Otegui M, Andrade F, Suero E (1995) Growth, water use, and kernel abortion of maize subjected to drought at silking. Field Crops Res 40:87–94
Oury V, Tardieu F, Turc O (2016) Ovary apical abortion under water deficit is caused by changes in sequential development of ovaries and in silk growth rate in maize. Plant Phyisol 171:986–996
Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150
Ruan Y-L, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012) Molecular regulation of seed and fruit set. Trends Plant Sci 17:656–665
Savadi S (2018) Molecular regulation of seed development and strategies for engineering seed size in crop plants. Plant Growth Regul 84:401–422
Schussler JR, Westgate ME (1994) Increasing assimilate reserves does not prevent kernel abortion at low water potential in maize. Crop Sci 34:1569
Setter TL, Flannigan BA, Melkonian J (2001) Loss of kernel set due to water deficit and shade in maize. Crop Sci 41:1530–1540
Shen S, Zhang L, Liang X-G, Zhao X, Lin S, Qu L-H, Liu Y-P, Gao Z, Ruan Y-L, Zhou S-L (2018) Delayed pollination and low availability of assimilates are major factors causing maize kernel abortion. J Exp Bot 69:1599–1613
Shen S, Liang X-G, Zhang L, Zhao X, Liu Y-P, Lin S, Gao Z, Wang P, Wang Z-M, Zhou S-L (2020) Intervening in sibling competition for assimilates by controlled pollination prevents seed abortion under postpollination drought in maize. Plant Cell Environ. https://doi.org/10.1111/pce.13704
Shi J, Gao H, Wang H, Lafitte HR, Archibald RL, Yang M, Hakimi SM, Mo H, Habben JE (2017) ARGOS8 variants generated by CRISPR-Cas9 improve maize grain yield under field drought stress conditions. Plant Biotech J 15:207–216
Turc O, Tardieu F (2018) Drought affects abortion of reproductive organs by exacerbating developmentally driven processes via expansive growth and hydraulics. J Exp Bot 69:3245–3254
Uribelarrea M, Cárcova J, Borrás L, Otegui ME (2008) Enhanced kernel set promoted by synchronous pollination determines a tradeoff between kernel number and kernel weight in temperate maize hybrids. Field Crops Res 105:172–181
Wang Y, Zhang C, Wang X, Wang W, Dong L (2014) Involvement of glucose in the regulation of ethylene biosynthesis and sensitivity in cut Paeonia suffruticosa flowers. Sci Hort 169:44–50
Wang Y, Tao H, Tian B, Sheng D, Xu C, Zhou H, Huang S, Wang P (2019) Flowering dynamics, pollen, and pistil contribution to grain yield in response to high temperature during maize flowering. Environ Exp Bot 158:80–88
Wang Z, Xu Y, Wang J, Yang J, Zhang J (2011) Polyamine and ethylene interactions in grain filling of superior and inferior spikelets of rice. Plant Growth Regul 66:215–228
Yang J, Zhang J, Liu K, Wang Z, Liu L (2006a) Abscisic acid and ethylene interact in wheat grains in response to soil drying during grain filling. New Phytol 171:293–303
Yang J, Zhang J, Wang Z, Liu K, Wang P (2006b) Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene. J Exp Bot 57:149–160
Young TE, Gallie DR, DeMason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Phyisol 115:737–751
Zhang CX, Feng BH, Chen TT, Zhang XF, Tao LX, Fu GF (2017a) Sugars, antioxidant enzymes and IAA mediate salicylic acid to prevent rice spikelet degeneration caused by heat stress. Plant Growth Regul 83:313–323
Zhang L, Li X-H, Gao Z, Shen S, Liang X-G, Zhao X, Lin S, Zhou S-L (2017b) Regulation of maize kernel weight and carbohydrate metabolism by abscisic acid applied at the early and middle post-pollination stages in vitro. J Plant Physiol 216:1–10
Zhang L, Liang X-G, Shen S, Yin H, Zhou L-L, Gao Z, Lv X-Y, Zhou S-L (2018) Increasing the abscisic acid level in maize grains induces precocious maturation by accelerating grain filling and dehydration. Plant Growth Regul 86:65–79
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant Nos. 31371558 and 31901435), the National Key Research and Development Program of China (Grant No. 2016YFD0300301), the China Agriculture Research System (Grant No. CARS-02-13), and the China Postdoctoral Science Foundation (Grant No. 2019M650900).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shen, S., Li, BB., Deng, T. et al. The equilibrium between sugars and ethylene is involved in shading- and drought-induced kernel abortion in maize. Plant Growth Regul 91, 101–111 (2020). https://doi.org/10.1007/s10725-020-00590-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-020-00590-8