Recent Advances on Plant Root Thermomorphogenesis

doi:10.7525/j.issn.1673-5102.2024.01.001

Abstract

Abstract:

Plant development is highly plastic. As ambient temperature increased， plant stems and petioles elongated， and promoted leaf surface cooling， the process known as thermomorphogenesis. High temperatures also triggered root elongation， which named as root thermomorphogenesis. There were many studies on the regulation of plant shoot thermomorphogenesis， but few investigations on the regulatory mechanisms of plant root thermomorphogenesis. In this review， we summarized the recent progresses in the field of plant root thermomorphogenesis， and proposed future research directions.

Key words: Arabidopsis thaliana, high temperature, root thermomorphogenesis, plant hormones

CLC Number:

Q944.54

Wei LIU, Ziqiang ZHU. Recent Advances on Plant Root Thermomorphogenesis[J]. Bulletin of Botanical Research, 2024, 44(1): 1-7.

Figures/Tables 1

References 54

1	VU L D， XU X Y， GEVAERT K，et al.Developmental plasticity at high temperature［J］.Plant Physiology，2019，181（2）：399-411.
2	QUINT M， DELKER C， FRANKLIN K A，et al.Molecular and genetic control of plant thermomorphogenesis［J］.Nature Plants，2016，2：15190.
3	CRAWFORD A J， MCLACHLAN D H， HETHERINGTON A M，et al.High temperature exposure increases plant cooling capacity［J］.Current Biology，2012，22（10）：R396-R397.
4	KOEVOETS I T， VENEMA J H， ELZENGA J T M，et al.Roots withstanding their environment：exploiting root system architecture responses to abiotic stress to improve crop tolerance［J］.Frontiers in Plant Science，2016，7：1335.
5	ZHAO C， LIU B， PIAO S L，et al.Temperature increase reduces global yields of major crops in four independent estimates［J］.Proceedings of the National Academy of Sciences of the United States of America，2017，114（35）：9326-9331.
6	赵恩博.1981—2016年蒙古国气温变化特征研究［J］.气候变化研究快报，2022，11（5）：820-829.
	ZHAO E B.The study on the characteristics of temperature change in Mongolia from 1981 to 2016［J］.Climate Change Research Letters，2022，11（5）：820-829.
7	YEH C H， KAPLINSKY N J， HU C，et al.Some like it hot，some like it warm：phenotyping to explore thermotolerance diversity［J］.Plant Science，2012，195：10-23.
8	LING Y， SERRANO N， GAO G，et al.Thermopriming triggers splicing memory in Arabidopsis ［J］.Journal of Experimental Botany，2018，69（10）：2659-2675.
9	SEDAGHATMEHR M， MUELLER-ROEBER B， BALAZADEH S.The plastid metalloprotease FtsH6 and small heat shock protein HSP21 jointly regulate thermomemory in Arabidopsis ［J］.Nature Communications，2016，7：12439.
10	MARTINS S， MONTIEL-JORDA A， CAYREL A，et al.Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature［J］.Nature Communications，2017，8（1）：309.
11	GRAY W M， ÖSTIN A， SANDBERG G，et al.High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis ［J］.Proceedings of the National Academy of Sciences of the United States of America，1998，95（12）：7197-7202.
12	LIN J Y， XU Y， ZHU Z Q.Emerging plant thermosensors：from RNA to protein［J］.Trends in Plant Science，2020，25（12）：1187-1189.
13	JUNG J H， SEO P J，OH E，et al.Temperature perception by plants［J］.Trends in Plant Science，2023，28（8）：924-940.
14	JUNG J H， DOMIJAN M， KLOSE C，et al.Phytochromes function as thermosensors in Arabidopsis ［J］.Science，2016，354（6314）：886-889.
15	LEGRIS M， KLOSE C， BURGIE E S，et al.Phytochrome B integrates light and temperature signals in Arabidopsis ［J］.Science，2016，354（6314）：897-900.
16	CHUNG B Y W， BALCEROWICZ M， DI ANTONIO M，et al.An RNA thermoswitch regulates daytime growth in Arabidopsis ［J］.Nature Plants，2020，6（5）：522-532.
17	NUSINOW D A， HELFER A， HAMILTON E E，et al.The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth［J］.Nature，2011，475（7356）：398-402.
18	SILVA C S， NAYAK A， LAI X L，et al.Molecular mechanisms of Evening Complex activity in Arabidopsis ［J］.Proceedings of the National Academy of Sciences of the United States of America，2020，117（12）：6901-6909.
19	HERRERO E， KOLMOS E， BUJDOSO N，et al.EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock［J］.The Plant Cell，2012，24（2）：428-443.
20	JUNG J H， BARBOSA A D， HUTIN S，et al.A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis ［J］.Nature，2020，585（7824）：256-260.
21	HALTENHOF T， KOTTE A， DE BORTOLI F，et al.A conserved kinase-based body-temperature sensor globally controls alternative splicing and gene expression［J］.Molecular Cell，2020，78（1）：57-69.e4.
22	LIN J Y， SHI J J， ZHANG Z H，et al.Plant AFC2 kinase desensitizes thermomorphogenesis through modulation of alternative splicing［J］.iScience，2022，25（4）：104051.
23	FRANKLIN K A， LEE S H， PATEL D，et al.Phytochrome-interacting factor 4 （PIF4） regulates auxin biosynthesis at high temperature［J］.Proceedings of the National Academy of Sciences of the United States of America，2011，108（50）：20231-20235.
24	SUN J Q， QI L L， LI Y N，et al.PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth［J］.PLoS Genetics，2012，8（3）：e1002594.
25	BELLSTAEDT J， TRENNER J， LIPPMANN R，et al.A mobile auxin signal connects temperature sensing in cotyledons with growth responses in hypocotyls［J］.Plant Physiology，2019，180（2）：757-766.
26	HANZAWA T， SHIBASAKI K， NUMATA T，et al.Cellular auxin homeostasis under high temperature is regulated through a sorting NEXIN1-dependent endosomal trafficking pathway［J］.The Plant Cell，2013，25（9）：3424-3433.
27	WANG R H， ZHANG Y， KIEFFER M，et al.HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1［J］.Nature Communications，2016，7（1）：10269.
28	AI H Y， BELLSTAEDT J， BARTUSCH K S，et al.Auxin‐dependent regulation of cell division rates governs root thermomorphogenesis［J］.The EMBO Journal，2023，42（11）：e111926.
29	QIU Y J， PASORECK E K， YOO C Y，et al.RCB initiates Arabidopsis thermomorphogenesis by stabilizing the thermoregulator PIF4 in the daytime［J］.Nature Communications，2021，12（1）：2042.
30	LEE S， WANG W L，HUQ E.Spatial regulation of thermomorphogenesis by HY5 and PIF4 in Arabidopsis ［J］.Nature Communications，2021，12（1）：3656.
31	CHEN X B， YAO Q F， GAO X H，et al.Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition［J］.Current Biology，2016，26（5）：640-646.
32	VAN GELDEREN K， KANG C， PAALMAN R，et al.Far-red light detection in the shoot regulates lateral root development through the HY5 transcription factor［J］.The Plant Cell，2018，30（1）：101-116.
33	GAILLOCHET C， BURKO Y， PLATRE M P，et al.HY5 and phytochrome activity modulate shoot-to-root coordination during thermomorphogenesis in Arabidopsis ［J］.Development，2020，147（24）：dev192625.
34	BORNIEGO M B， COSTIGLIOLO-ROJAS C， CASAL J J.Shoot thermosensors do not fulfil the same function in the root［J］.The New Phytologist，2022，236（1）：9-14.
35	FIORUCCI A S， GALVÃO V C， INCE Y Ç，et al.PHYTOCHROME INTERACTING FACTOR 7 is important for early responses to elevated temperature in Arabidopsis seedlings［J］.The New Phytologist，2020，226（1）：50-58.
36	DE LIMA C F F， KLEINE-VEHN J， DE SMET I，et al.Getting to the root of belowground high temperature responses in plants［J］.Journal of Experimental Botany，2021，72（21）：7404-7413.
37	FERARU E， FERARU M I， BARBEZ E，et al.PILS6 is a temperature-sensitive regulator of nuclear auxin input and organ growth in Arabidopsis thaliana ［J］.Proceedings of the National Academy of Sciences of the United States of America，2019，116（9）：3893-3898.
38	IBAÑEZ C， POESCHL Y， PETERSON T，et al.Ambient temperature and genotype differentially affect developmental and phenotypic plasticity in Arabidopsis thaliana ［J］.BMC Plant Biology，2017，17（1）：114.
39	YANG X L， DONG G， PALANIAPPAN K，et al.Temperature-compensated cell production rate and elongation zone length in the root of Arabidopsis thaliana ［J］.Plant，Cell & Environment，2017，40（2）：264-276.
40	KEPINSKI S， LEYSER O.The Arabidopsis F-box protein TIR1 is an auxin receptor［J］.Nature，2005，435（7041）：446-451.
41	BARBEZ E， KUBEŠ M， ROLČÍK J，et al.A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants［J］.Nature，2012，485（7396）：119-122.
42	BÉZIAT C， BARBEZ E， FERARU M I，et al.Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition［J］.Nature Plants，2017，3：17105.
43	GRIF V G， VALOVICH E M.Effect of low positive temperatures on cell growth and division during seed development［J］.Tsitologiia，1973，15（11）：1362-1369.
44	MURÍN A.The effect of temperature on the mitotic cycle and its time parameters in root tips of Vicia faba ［J］.Naturwissenschaften，1966，53（12）：312-313.
45	SILK W K， LORD E M， ECKARD K J.Growth patterns inferred from anatomical records：empirical tests using longisections of roots of Zea mays L ［J］.Plant Physiology，1989，90（2）：708-713.
46	GONZÁLEZ-GARCÍA M P， VILARRASA-BLASI J， ZHIPONOVA M，et al.Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots［J］.Development，2011，138（5）：849-859.
47	HACHAM Y， HOLLAND N， BUTTERFIELD C，et al.Brassinosteroid perception in the epidermis controls root meristem size［J］.Development，2011，138（5）：839-848.
48	FRIDMAN Y， ELKOUBY L， HOLLAND N，et al.Root growth is modulated by differential hormonal sensitivity in neighboring cells［J］.Genes & Development，2014，28（8）：912-920.
49	SUN L， FERARU E， FERARU M I，et al.PIN-LIKES coordinate brassinosteroid signaling with nuclear auxin input in Arabidopsis thaliana ［J］.Current Biology，2020，30（9）：1579-1588.e6.
50	RŮŽIČKA K， LJUNG K， VANNESTE S，et al.Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution［J］.The Plant Cell，2007，19（7）：2197-2212.
51	ZEMLYANSKAYA E V， OMELYANCHUK N A， UBOGOEVA E V，et al.Deciphering auxin-ethylene crosstalk at a systems level［J］.International Journal of Molecular Sciences，2018，19（12）：4060.
52	STREET I H， AMAN S， ZUBO Y，et al.Ethylene inhibits cell proliferation of the Arabidopsis root meristem［J］.Plant Physiology，2015，169（1）：338-350.
53	FEI Q H， WEI S D， ZHOU Z Y，et al.Adaptation of root growth to increased ambient temperature requires auxin and ethylene coordination in Arabidopsis ［J］.Plant Cell Reports，2017，36（9）：1507-1518.
54	BODEN S A， KAVANOVÁ M， FINNEGAN E J，et al.Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A.Z-nucleosomes［J］.Genome Biology，2013，14（6）：R65.

[1]	Zhuanzhuan JIANG, Li GONG, Yaling SONG. The Chloroplast Division Protein PARC6 Affected the Growth of Cotyledon and Leaf in Arabidopsis thaliana [J]. Bulletin of Botanical Research, 2023, 43(5): 700-710.
[2]	Sheng ZHENG, Haixia GAO, Min SU, Shanghuan LU, Tengguo ZHANG, Guofan WU. Exogenous Sucrose Affected AtKEA1 and AtKEA2 to Regulate Root Growth of Seedling in Arabidopsis thaliana [J]. Bulletin of Botanical Research, 2023, 43(4): 562-571.
[3]	Yuping QIU, Yichuan WANG, Hongwei GUO. Research Progress on the Regulatory Mechanism of Plant Root Hair Development [J]. Bulletin of Botanical Research, 2023, 43(3): 321-332.
[4]	Yuanyuan CAI, Jibenben XIA, Wenhan YING, Jieyao WANG, Tao XIE, Kongya XING, Xuanjun FENG, Xuejun HUA. Detailed Phenotypical Analysis on the Mutant ssr1-2 Encoding a Mitochondrial Protein of Arabidopsis thaliana [J]. Bulletin of Botanical Research, 2023, 43(3): 421-431.
[5]	Kun CHEN, Gonggui FANG, Huaizhi MU, Jing JIANG. Analysis of the Promoter Sequence and Response Characteristics of the BpPIN3 gene in Betula platyphylla [J]. Bulletin of Botanical Research, 2022, 42(4): 592-601.
[6]	Mengjiao Wang, Yuxue Cao, Yongsheng Xu, Fenge Ding, Qiao Su. Overexpression of Marine Microbial Metagenomic MbCSP Enhanced Drought and Cold Tolerance of Transgenic Arabidopsisthaliana [J]. Bulletin of Botanical Research, 2022, 42(2): 243-251.
[7]	Yun-Hao ZHU, Meng-Jia ZHANG, Cheng-Ming DONG. Effects of Exogenous MeJA on Antioxidant System and Stress Genes of Pinellia ternata under High Temperature Stress [J]. Bulletin of Botanical Research, 2021, 41(1): 67-73.
[8]	LIU Jin-Yu, GAO Yue-Hao, HUANG Jin-Shuo, ZHANG Qin. Effects of Exogenous Salicylic Acid on Physiological and Electrical Impedance Parameters of Trollius chinensis Seedlings under High Temperature Stress [J]. Bulletin of Botanical Research, 2020, 40(4): 543-551.
[9]	ZHANG Yu-Qing, LIU Ye, QU Chun-Pu, LIU Guan-Jun, YANG Tian-Tian, YANG Cheng-Jun. Resistance Analysis of Transgenic PnDof30 Arabidopsis under Abiotic Stress [J]. Bulletin of Botanical Research, 2020, 40(3): 407-415.
[10]	LI Zi-Yi, HE Zi-Hang, LU Hui-Jun, WANG Yu-Cheng, JI Xiao-Yu. Study on Salt Tolerance of AtUNE12 Gene in Arabidopsis thaliana [J]. Bulletin of Botanical Research, 2020, 40(2): 257-265.
[11]	HE Hao, ZHU Guo-Qing, CHEN Shi-Ya, XU Chang, JIN Shu-Mei. Cloning of LpPEX7 Gene from Lilium pumilum and Its Expression Characteristics under Salt Stress [J]. Bulletin of Botanical Research, 2020, 40(2): 274-283.
[12]	WANG Shuang, CHENG Yu-Xiang, XIA De-An. Identification of Key Amino Acid Sites in AtGDPD-Like3 with Role in Arabidopsis Root Hairs [J]. Bulletin of Botanical Research, 2020, 40(1): 79-84.
[13]	LI Peng, HUAN Zhao-Wei, DING Lan. Rabdosinate Regulates Polar Auxin Carriers PIN1,PIN3 and PIN4 and Inhibits Root Growth of Arabidopsis thaliana Seedlings [J]. Bulletin of Botanical Research, 2019, 39(6): 908-916.
[14]	FAN Er-Qin, LIU Cai-Xia, FU Peng-Yue, YANG Chuan-Ping, QU Guan-Zheng. Expression Pattern of PagC3H3 Gene in Populus alba×P.glandulosa [J]. Bulletin of Botanical Research, 2019, 39(4): 521-528.
[15]	ZHAO Min, WANG Yue-Xuan, XU Yun-Fei, ZHAO Qi-An, LIU Bo, YANG Ning. Relationship between H₂S and ABA Signaling in Arabidopsis thaliana under Drought Stress [J]. Bulletin of Botanical Research, 2019, 39(1): 104-112.