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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Habanero pepper (Capsicum chinense) adaptation to water-deficit stress in a protected agricultural system

Alejandra Nieto-Garibay A , Aarón Barraza B , Goretty Caamal-Chan B , Bernardo Murillo-Amador A , Enrique Troyo-Diéguez A , Carlos Alexis Burgoa-Cruz C , Jhesy Nury Jaramillo-Limón D and Abraham Loera-Muro https://orcid.org/0000-0002-3163-1847 B *
+ Author Affiliations
- Author Affiliations

A Centro de Investigaciones Biológicas del Noroeste, SC, Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur, C.P. 23096, La Paz, Baja California Sur, Mexico.

B CONACYT-Centro de Investigaciones Biológicas del Noroeste, SC, Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur, La Paz, Baja California Sur, C.P. 23096, Mexico.

C Instituto Tecnológico de La Paz, Boulevard Forjadores de Baja California Sur 4720, 8 de Octubre 2da Secc, La Paz, Baja California Sur, C.P. 23080, Mexico.

D Universidad de Occidente, Unidad los Mochis Boulevard Macario Gaxiola SN Col. Las Malvinas, C.P. 81216, Los Mochis, Sinaloa, Mexico.

* Correspondence to: aloera@cibnor.mx

Handling Editor: Manuela Chaves

Functional Plant Biology 49(3) 295-306 https://doi.org/10.1071/FP20394
Submitted: 17 December 2020  Accepted: 11 January 2022   Published: 8 February 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Drought is one of the major factors limiting global crop yield. In Mexico, agriculture is expected to be severely affected by drought. The Capsicum genus has several crop species of agricultural importance. In this work, we analysed the Capsicum chinense plant physiological responses and differentially expressed genes under water stress mainly focused on the responses elicited following recovery through repetitive stress. Plants were cultivated in an experimental block. Each block consisted of plants under water deficit and a control group without deficit. Morphometric and functional parameters, and the expression of genes related to resistance to abiotic stresses were measured. Morphological differences were observed. Plants subjected to water deficit showed impaired growth. Nonetheless, in the physiological parameters, no differences were observed between treatments. We selected abiotic stress-related genes that include heat-shock proteins (HSPs), heat-shock factors (HSFs), transcription factors related to abiotic stress (MYB, ETR1, and WRKY), and those associated with biotic and abiotic stress responses (Jar1 and Lox2). HSF, HSP, MYB72, ETR1, Jar1, WRKYa, and Lox2 genes were involved in the response to water-deficit stress in C. chinense plants. In conclusion, our work may improve our understanding of the morphological, physiological, and molecular mechanisms underlying hydric stress response in C. chinense.

Keywords: abiotic stress, abiotic stress-related genes, Capsicum chinense, drought, heat shock factor, heat shock protein, protected agricultural system, water-deficit stress.


References

Aneja B, Yadav NR, Kumar N, Yadav RC (2015) HSP transcript induction is correlated with physiological changes under drought stress in Indian mustard. Physiology and Molecular Biology of Plants 21, 305–316.
HSP transcript induction is correlated with physiological changes under drought stress in Indian mustard.Crossref | GoogleScholarGoogle Scholar | 26261395PubMed |

Arnon D (1949) Copper enzymes isolated chloroplasts, polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
Copper enzymes isolated chloroplasts, polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 16654194PubMed |

Ashraf MF, Yang S, Wu R, Wang Y, Hussain A, Noman A, Khan MI, Liu Z, Qiu A, Guan D, He S (2018) Capsicum annuum HsfB2a positively regulates the response to Ralstonia solanacearum infection or high temperature and high humidity forming transcriptional cascade with CaWRKY6 and CaWRKY40. Plant Cell Physiology 59, 2608–2623.
Capsicum annuum HsfB2a positively regulates the response to Ralstonia solanacearum infection or high temperature and high humidity forming transcriptional cascade with CaWRKY6 and CaWRKY40.Crossref | GoogleScholarGoogle Scholar | 30169791PubMed |

Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes 10, 771
Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement.Crossref | GoogleScholarGoogle Scholar |

Bakshi M, Oelmüller R (2014) WRKY Transcription Factors: Jack of many trades in plants. Plant Signaling & Behavior 9, e27700
WRKY Transcription Factors: Jack of many trades in plants.Crossref | GoogleScholarGoogle Scholar |

Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
Photosynthetic response and adaptation to temperature in higher plants.Crossref | GoogleScholarGoogle Scholar |

Chen J, Gao T, Wan S, Zhang Y, Yang J, Yu Y, Wang W (2018) Genome-wide identification, classification and expression analysis of the HSP gene superfamily in tea plant (Camellia sinensis). International Journal of Molecular Sciences 19, 2633
Genome-wide identification, classification and expression analysis of the HSP gene superfamily in tea plant (Camellia sinensis).Crossref | GoogleScholarGoogle Scholar |

Clauw P, Coppens F, De Beuf K, Dhondt S, Van Daele T, Maleux K, Storme V, Clement L, Gonzalez N, Inzé D (2015) Leaf responses to mild drought stress in natural variants of Arabidopsis. Plant Physiology 167, 800–816.
Leaf responses to mild drought stress in natural variants of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25604532PubMed |

CONAGUA (2020) Available at https://smn.conagua.gob.mx/es/climatologia/temperaturas-y-lluvias/resumenes-mensuales-de-temperaturas-y-lluvias) Comisión Nacional de Agua.

Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species. Plant Signaling & Behavior 3, 156–165.
Drought stress and reactive oxygen species.Crossref | GoogleScholarGoogle Scholar |

Dang F-F, Wang Y-N, Yu L, et al. (2013) CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant, Cell & Environment 36, 757–774.
CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection.Crossref | GoogleScholarGoogle Scholar |

De Domenico S, Bonsegna S, Horres R, Pastor V, Taurino M, Poltronieri P, Imtiaz M, Kahl G, Flors V, Winter P, Santino A (2012) Transcriptomic analysis of oxylipin biosynthesis genes and chemical profiling reveal an early induction of jasmonates in chickpea roots under drought stress. Plant Physiology and Biochemistry 61, 115–122.
Transcriptomic analysis of oxylipin biosynthesis genes and chemical profiling reveal an early induction of jasmonates in chickpea roots under drought stress.Crossref | GoogleScholarGoogle Scholar | 23141673PubMed |

de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A (2020) Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368, 270–274.
Harnessing rhizosphere microbiomes for drought-resilient crop production.Crossref | GoogleScholarGoogle Scholar | 32299947PubMed |

Ding Y, Liu N, Virlouvet L, Riethoven J-J, Fromm M, Avramova Z (2013) Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biology 13, 229
Four distinct types of dehydration stress memory genes in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 24377444PubMed |

Driedonks N, Xu J, Peters JL, Park S, Rieu I (2015) Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat. Frontiers in Plant Science 6, 999
Multi-level interactions between heat shock factors, heat shock proteins, and the redox system regulate acclimation to heat.Crossref | GoogleScholarGoogle Scholar | 26635827PubMed |

Du Y, Zhao Q, Chen L, Yao X, Zhang W, Zhang B, Xie F (2020) Effect of drought stress on sugar metabolism in leaves and roots of soybean seedlings. Plant Physiology and Biochemistry 146, 1–12.
Effect of drought stress on sugar metabolism in leaves and roots of soybean seedlings.Crossref | GoogleScholarGoogle Scholar | 31710920PubMed |

El-Esawi MA, Al-Ghamdi AA, Ali HM, Ahmad M (2019) Overexpression of AtWRKY30 transcription factor enhances heat and drought stress tolerance in wheat (Triticum aestuvum L.). Genes 10, 163
Overexpression of AtWRKY30 transcription factor enhances heat and drought stress tolerance in wheat (Triticum aestuvum L.).Crossref | GoogleScholarGoogle Scholar |

Fan F, Yang X, Cheng Y, Kang Y, Chai X (2017) The DnaJ gene family in pepper (Capsicum annuum L.): comprehensive identification, characterization and expression profiles. Frontiers in Plant Science 8, 689
The DnaJ gene family in pepper (Capsicum annuum L.): comprehensive identification, characterization and expression profiles.Crossref | GoogleScholarGoogle Scholar | 28507559PubMed |

Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cellular and Molecular Life Sciences 72, 673–689.
General mechanisms of drought response and their application in drought resistance improvement in plants.Crossref | GoogleScholarGoogle Scholar | 25336153PubMed |

Feng X-H, Zhang H-X, Ali M, Gai W-X, Cheng G-X, Yu Q-H, Yang S-B, Li X-X, Gong Z-H (2019) A small heat shock protein CaHsp25.9 positively regulates heat, salt, and drought stress tolerance in pepper (Capsicum annuum L.). Plant Physiology and Biochemistry 142, 151–162.
A small heat shock protein CaHsp25.9 positively regulates heat, salt, and drought stress tolerance in pepper (Capsicum annuum L.).Crossref | GoogleScholarGoogle Scholar | 31284139PubMed |

Gao H, Wang Y, Xu P, Zhang Z (2018) Overexpression of a WRKY transcription factor TaWRKY2 enhances drought stress tolerance in transgenic wheat. Frontiers in Plant Science 9, 997
Overexpression of a WRKY transcription factor TaWRKY2 enhances drought stress tolerance in transgenic wheat.Crossref | GoogleScholarGoogle Scholar | 30131813PubMed |

Gigon A, Matos A-R, Laffray D, Zuily-Fodil Y, Pham-Thi A-T (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (Ecotype Columbia). Annals of Botany 94, 345–351.
Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (Ecotype Columbia).Crossref | GoogleScholarGoogle Scholar | 15277243PubMed |

Goodarzian Ghahfarokhi M, Mansurifar S, Taghizadeh-Mehrjardi R, Saeidi M, Jamshidi AM, Ghasemi E (2015) Effects of drought stress and rewatering on antioxidant systems and relative water content in different growth stages of maize (Zea mays L.) hybrids. Archives of Agronomy and Soil Science 61, 493–506.
Effects of drought stress and rewatering on antioxidant systems and relative water content in different growth stages of maize (Zea mays L.) hybrids.Crossref | GoogleScholarGoogle Scholar |

Gornall J, Betts R, Burke E, Clark R, Camp J, Willett K, Wiltshire A (2010) Implications of climate change for agricultural productivity in the early twenty first century. Philosophical Transactions of the Royal Society B 365, 2973–2989.
Implications of climate change for agricultural productivity in the early twenty first century.Crossref | GoogleScholarGoogle Scholar |

Guo M, Yin Y-X, Ji J-J, Ma B-P, Lu M-H, Gong Z-H (2014a) Cloning and expression analysis of heat-shock transcription factor gene CaHsfA2 from pepper (Capsicum annuum L.). Genetics and Molecular Research 13, 1865–1875.
Cloning and expression analysis of heat-shock transcription factor gene CaHsfA2 from pepper (Capsicum annuum L.).Crossref | GoogleScholarGoogle Scholar | 24668674PubMed |

Guo M, Zhai Y-F, Lu J-P, Chai L, Chai W-G, Gong Z-H, Lu M-H (2014b) Characterization of CaHsp70-1, a pepper heat-shock protein gene in response to heat stress and some regulation exogenous substances in Capsicum annuum L. International Journal of Molecular Sciences 15, 19741–19759.
Characterization of CaHsp70-1, a pepper heat-shock protein gene in response to heat stress and some regulation exogenous substances in Capsicum annuum L.Crossref | GoogleScholarGoogle Scholar | 25356507PubMed |

Guo M, Lu J-P, Zhai Y-F, Chai W-G, Gong Z-H, Lu M-H (2015) Genome-wide analysis, expression profile of heat shock factor gene family (CaHsfs) and characterization of CaHsfA2 in pepper (Capsicum annuum L.). BMC Plant Biology 15, 151
Genome-wide analysis, expression profile of heat shock factor gene family (CaHsfs) and characterization of CaHsfA2 in pepper (Capsicum annuum L.).Crossref | GoogleScholarGoogle Scholar | 26088319PubMed |

Guo M, Liu J-H, Ma X, Luo D-X, Gong Z-H, Lu M-H (2016) The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Frontiers in Plant Science 7, 114
The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 26904076PubMed |

Han K, Jang S, Lee J-H, Lee D-G, Kwon J-K, Kang B-C (2019) A MYB transcription factor is a candidate to control pungency in Capsicum annuum. Theoretical and Applied Genetics 132, 1235–1246.
A MYB transcription factor is a candidate to control pungency in Capsicum annuum.Crossref | GoogleScholarGoogle Scholar | 30607439PubMed |

Haq S, Khan A, Ali M, Gai W-X, Zhang H-X, Yu Q-H, Yang S-B, Wei A-M, Gong Z-H (2019) Knockdown of CaHSP60-6 confers enhanced sensitivity to heat stress in pepper (Capsicum annuum L.). Planta 250, 2127–2145.
Knockdown of CaHSP60-6 confers enhanced sensitivity to heat stress in pepper (Capsicum annuum L.).Crossref | GoogleScholarGoogle Scholar | 31606756PubMed |

Huang L-J, Cheng G-X, Khan A, Wei A-M, Yu Q-H, Yang S-B, Luo D-X, Gong Z-H (2019) CaHSP16.4, a small heat shock protein gene in pepper, is involved in heat and drought tolerance. Protoplasma 256, 39–51.
CaHSP16.4, a small heat shock protein gene in pepper, is involved in heat and drought tolerance.Crossref | GoogleScholarGoogle Scholar | 29946904PubMed |

Huh SU, Lee GJ, Jung JH, Kim Y, Kim YJ, Paek KH (2015) Capsicum annuum transcription factor WRKYa positively regulates defense response upon TMV infection and is a substrate of CaMK1 and CaMK2. Sci Rep 5, 7981
Capsicum annuum transcription factor WRKYa positively regulates defense response upon TMV infection and is a substrate of CaMK1 and CaMK2.Crossref | GoogleScholarGoogle Scholar | 25613640PubMed |

Hussain A, Noman A, Khan MI, et al. (2019) Molecular regulation of pepper innate immunity and stress tolerance: an overview of WRKY TFs. Microbial Pathogenesis 135, 103610
Molecular regulation of pepper innate immunity and stress tolerance: an overview of WRKY TFs.Crossref | GoogleScholarGoogle Scholar | 31288065PubMed |

Jacob P, Hirt H, Bendahmane A (2017) The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnology Journal 15, 405–414.
The heat-shock protein/chaperone network and multiple stress resistance.Crossref | GoogleScholarGoogle Scholar | 27860233PubMed |

Jin B, Wang L, Wang J, Jiang K-Z, Wang Y, Jiang X-X, Ni C-Y, Wang Y-L, Teng N-J (2011) The effect of experimental warming on leaf functional traits, leaf structure and leaf biochemistry in Arabidopsis thaliana. BMC Plant Biology 11, 35
The effect of experimental warming on leaf functional traits, leaf structure and leaf biochemistry in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21329528PubMed |

Kim NH, Hwang BK (2015) Pepper heat shock protein 70a interacts with the type III effector AvrBsT and triggers plant cell death and immunity. Plant Physiology 167, 307–322.
Pepper heat shock protein 70a interacts with the type III effector AvrBsT and triggers plant cell death and immunity.Crossref | GoogleScholarGoogle Scholar | 25491184PubMed |

Lee S, Choi D (2013) Comparative transcriptome analysis of pepper (Capsicum annuum) revealed common regulons in multiple stress conditions and hormone treatments. Plant Cell Reports 32, 1351–1359.
Comparative transcriptome analysis of pepper (Capsicum annuum) revealed common regulons in multiple stress conditions and hormone treatments.Crossref | GoogleScholarGoogle Scholar | 23649878PubMed |

Li T, Xu X, Li Y, Wang H, Li Z, Li Z (2015) Comparative transcriptome analysis reveals differential transcription in heat-susceptible and heat-tolerant pepper (Capsicum annum L.) cultivars under heat stress. Journal of Plant Biology 58, 411–424.
Comparative transcriptome analysis reveals differential transcription in heat-susceptible and heat-tolerant pepper (Capsicum annum L.) cultivars under heat stress.Crossref | GoogleScholarGoogle Scholar |

Li P, Yang H, Wang L, Liu H, Huo H, Zhang C, Liu A, Zhu A, Hu J, Lin Y, Liu L (2019) Physiological and transcriptome analyses reveal short term responses and formation of memory under drought stress in rice. Frontiers in Genetics 10, 55
Physiological and transcriptome analyses reveal short term responses and formation of memory under drought stress in rice.Crossref | GoogleScholarGoogle Scholar | 30800142PubMed |

Lim CW, Han S-W, Hwang IS, Kim DS, Hwang BK, Lee SC (2015) The pepper Lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response. Plant and Cell Physiology 56, 930–942.
The pepper Lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response.Crossref | GoogleScholarGoogle Scholar | 25657344PubMed |

Lin Y-S, Medlyn BE, Ellsworth DS (2012) Temperature responses of leaf net photosynthesis: the role of component processes. Tree Physiology 32, 219–231.
Temperature responses of leaf net photosynthesis: the role of component processes.Crossref | GoogleScholarGoogle Scholar | 22278379PubMed |

Liu J, Wang R, Liu W, Zhang H, Guo Y, Wen R (2018) Genome-wide characterization of heat-shock protein 70s from Chenopodium quinoa and expression analyses of Cqhsp70s in response to drought stress. Genes (Basel) 9, 35

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Mathur S, Allakhverdiev SI, Jajoo A (2011) Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of Photosystem II in wheat leaves (Triticum aestivum). Biochimica et Biophysica Acta (BBA) - Bioenergetics 1807, 22–29.
Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of Photosystem II in wheat leaves (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar |

Moran JF, Becan M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stresses in pea plants. Planta 194, 346–352.
Drought induces oxidative stresses in pea plants.Crossref | GoogleScholarGoogle Scholar |

Murillo-Amador B, Morales-Prado LE, Troyo-Diéguez E, Córdoba-Matson MV, Hernández-Montiel LG, Rueda-Puente EO, Nieto-Garibay A (2015) Changing environmental conditions and applying organic fertilizers in Origanum vulgare L. Frontiers in Plant Science 6, 549
Changing environmental conditions and applying organic fertilizers in Origanum vulgare L.Crossref | GoogleScholarGoogle Scholar | 26257756PubMed |

Nieto-Garibay A, Murillo-Amador B, Troyo-Diéguez E, Reyes-Pérez J, Hernández-Montiel LG, Yescas PC (2016) Physiological strategies basil cultivars (Ocimum basilicum L.) under protected agriculture. Revista Mexicana de Ciencias Agrícolas 17, 3477–3490.

Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Transcriptional regulatory network of plant heat stress response. Trends in Plant Science 22, 53–65.
Transcriptional regulatory network of plant heat stress response.Crossref | GoogleScholarGoogle Scholar | 27666516PubMed |

Qin D, Wu H, Peng H, Yao Y, Ni Z, Li Z, Zhou C, Sun Q (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 9, 432
Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array.Crossref | GoogleScholarGoogle Scholar | 18808683PubMed |

Qu A-L, Ding Y-F, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochemical and Biophysical Research Communications 432, 203–207.
Molecular mechanisms of the plant heat stress response.Crossref | GoogleScholarGoogle Scholar | 23395681PubMed |

Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant, Cell & Environment 30, 1086–1106.
The temperature response of C3 and C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Reports 32, 1085–1098.
Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses.Crossref | GoogleScholarGoogle Scholar | 23584548PubMed |

Sarde SJ, Kumar A, Remme RN, Dicke M (2018) Genome-wide identification, classification and expression of Lipoxygenase gene family in pepper. Plant Molecular Biology 98, 375–387.
Genome-wide identification, classification and expression of Lipoxygenase gene family in pepper.Crossref | GoogleScholarGoogle Scholar | 30317456PubMed |

SIAP, Servicio de Información Agroalimentaria y Pesquería, SAGARPA (2019) Available at https://www.gob.mx/siap

Slatyer R (1967) ‘Plant-Water relationships’ (Academic Press: Cambridge, MA)

Sun J-T, Cheng G-X, Huang L-J, Liu S, Ali M, Abid K, Yu Q-H, Yang S-B, Luo D-X, Gong Z-H (2019a) Modified expression of a heat shock protein gene, CaHSP22.0, results in high sensitivity to heat and salt stress in pepper (Capsicum annuum L.). Scientia Horticulturae 249, 364–373.
Modified expression of a heat shock protein gene, CaHSP22.0, results in high sensitivity to heat and salt stress in pepper (Capsicum annuum L.).Crossref | GoogleScholarGoogle Scholar |

Sun B, Zhu Z, Chen C, Chen G, Cao B, Chen C, Lei J (2019b) Jasmonate-inducible R2R3-MYB Transcription Factor regulates capsaicinoid biosynthesis and stamen development in Capsicum. Journal of Agricultural and Food Chemistry 67, 10891–10903.
Jasmonate-inducible R2R3-MYB Transcription Factor regulates capsaicinoid biosynthesis and stamen development in Capsicum.Crossref | GoogleScholarGoogle Scholar | 31505929PubMed |

Tang Y, Bao X, Zhi Y, et al. (2019) Overexpression of a MYB family gene, OsMYB6, increases drought and salinity stress tolerance in transgenic rice. Frontiers in Plant Science 10, 168
Overexpression of a MYB family gene, OsMYB6, increases drought and salinity stress tolerance in transgenic rice.Crossref | GoogleScholarGoogle Scholar | 30833955PubMed |

Usman MG, Rafii MY, Martini MY, Yusuff OA, Ismail MR, Miah G (2018) Introgression of heat shock protein (Hsp70 and sHsp) genes into the Malaysian elite chilli variety Kulai (Capsicum annuum L.) through the application of marker-assisted backcrossing (MAB). Cell Stress and Chaperones 23, 223–234.
Introgression of heat shock protein (Hsp70 and sHsp) genes into the Malaysian elite chilli variety Kulai (Capsicum annuum L.) through the application of marker-assisted backcrossing (MAB).Crossref | GoogleScholarGoogle Scholar | 28812232PubMed |

Virlouvet L, Avenson TJ, Du Q, Zhang C, Liu N, Fromm M, Avramova Z, Russo SE (2018) dehydration stress memory: gene networks linked to physiological responses during repeated stresses of Zea mays. Frontiers in Plant Science 9, 1058
dehydration stress memory: gene networks linked to physiological responses during repeated stresses of Zea mays.Crossref | GoogleScholarGoogle Scholar | 30087686PubMed |

Wan H, Yuan W, Ruan M, Ye Q, Wang R, Li Z, Zhou G, Yao Z, Zhao J, Liu S, Yang Y (2011) Identification of reference genes for reverse transcription quantitative real-time PCR normalization in pepper (Capsicum annuum L.). Biochemical and Biophysical Research Communications 416, 24–30.
Identification of reference genes for reverse transcription quantitative real-time PCR normalization in pepper (Capsicum annuum L.).Crossref | GoogleScholarGoogle Scholar | 22086175PubMed |

Wang X, Cai J, Jiang D, Liu F, Dai T, Cao W (2011) Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. Journal of Plant Physiology 168, 585–593.
Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat.Crossref | GoogleScholarGoogle Scholar | 21247658PubMed |

Wang G, Cai G, Xu N, Zhang L, Sun X, Guan J, Meng Q (2019a) Novel DnaJ protein facilitates thermotolerance of transgenic tomatoes. International Journal of Molecular Sciences 20, 367
Novel DnaJ protein facilitates thermotolerance of transgenic tomatoes.Crossref | GoogleScholarGoogle Scholar |

Wang J, Lv J, Liu Z, Liu Y, Song J, Ma Y, Ou L, Zhang X, Liang C, Wang F, Juntawong N, Jiao C, Chen W, Zou X (2019b) Integration of transcriptomics and metabolomics for pepper (Capsicum annuum L.) in response to heat stress. International Journal of Molecular Sciences 20, 5042
Integration of transcriptomics and metabolomics for pepper (Capsicum annuum L.) in response to heat stress.Crossref | GoogleScholarGoogle Scholar |

Yamada M, Morishita H, Urano K, Shiozaki N, Yamaguchi-Shinozaki K, Shinozaki K, Yoshiba Y (2005) Effects of free proline accumulation in petunias under drought stress. Journal of Experimental Botany 56, 1975–1981.
Effects of free proline accumulation in petunias under drought stress.Crossref | GoogleScholarGoogle Scholar | 15928013PubMed |

Yang X-Y, Jiang W-J, Yu H-J (2012) The expression profiling of the Lipoxygenase (LOX) family genes during fruit development, abiotic stress and hormonal treatments in cucumber (Cucumis sativus L.). International Journal of Molecular Sciences 13, 2481–2500.
The expression profiling of the Lipoxygenase (LOX) family genes during fruit development, abiotic stress and hormonal treatments in cucumber (Cucumis sativus L.).Crossref | GoogleScholarGoogle Scholar | 22408466PubMed |

Yang X, Zhu W, Zhang H, Liu N, Tian S (2016) Heat shock factors in tomatoes: genome-wide identification, phylogenetic analysis and expression profiling under development and heat stress. PeerJ 4, e1961
Heat shock factors in tomatoes: genome-wide identification, phylogenetic analysis and expression profiling under development and heat stress.Crossref | GoogleScholarGoogle Scholar | 27190703PubMed |

Ye S, Yu S, Shu L, Wu J, Wu A, Luo L (2012) Expression profile analysis of 9 heat shock protein genes throughout the life cycle and under abiotic stress in rice. Chinese Science Bulletin 57, 336–343.
Expression profile analysis of 9 heat shock protein genes throughout the life cycle and under abiotic stress in rice.Crossref | GoogleScholarGoogle Scholar |

Yildizli A, Çevik S, Ünyayar S (2018) Effects of exogenous myo-inositol on leaf water status and oxidative stress of Capsicum annuum under drought stress. Acta Physiologiae Plantarum 40, 122
Effects of exogenous myo-inositol on leaf water status and oxidative stress of Capsicum annuum under drought stress.Crossref | GoogleScholarGoogle Scholar |

Zhu Z, Xu X, Cao B, Chen C, Chen Q, Xiang C, Chen G, Lei J (2015) Pyramiding of AtEDT1/HDG11 and Cry2Aa2 into pepper (Capsicum annuum L.) enhances drought tolerance and insect resistance without yield decrease. Plant Cell, Tissue and Organ Culture (PCTOC) 120, 919–932.
Pyramiding of AtEDT1/HDG11 and Cry2Aa2 into pepper (Capsicum annuum L.) enhances drought tolerance and insect resistance without yield decrease.Crossref | GoogleScholarGoogle Scholar |