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Hydrogen Sulfide in Root Development: Comparison
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Please note this is a comparison between Version 2 by Jason Zhu and Version 1 by Hua Li.

Hydrogen sulfide (H2S) is regarded as a “New Warrior” for managing plant stress. ItHydrogen also plays an important role in plansulfide has a concentration-dependent effect on the regulation of root growth and development. 

  • Hydrogen Sulfide
  • Root
  • Growth

1. Hydrogen Sulfide Regulates the Formation and Growth of Lateral and Adventitious Roots

Hydrogen sulfide has a concentration-dependent effect on the regulation of root growth. In tomato, 0.01–1.0 mM sodium hydrosulfide (NaHS) (a H2S donor) can significantly promote the initiation and length of lateral roots (LRs) and can increase the number and density of LRs. However, a high concentration of NaHS (10 mM) inhibits the LRs’ growth [23][1]. A similar phenomenon was found in the mangrove plant Kandelia obovata, where a concentration of 0.01–1.0 mM NaHS led to a notable increase in the length and total surface area of LRs [27][2]. H2S was essential for the formation of pepper LRs, where a concentration of 0.5–8.0 mM NaHS significantly increased the number of LRs. In contrast, different concentrations of the H2S scavenger hypotaurine (HT) markedly inhibited the formation of LRs [24][3]. In peach, H2S had a notable effect on the formation of LRs, with a concentration of 0.2 mM NaHS leading to a significant increase in the number of LRs [33][4]. Our previous research also found that H2S promoted the growth and development of lateral roots in wheat, with a concentration of 0.4 mM NaHS resulting in an increase in the number, density, and length of LRs [35]. However, in Arabidopsis, the effects of H2S on lateral roots were slightly different. H2S can promote the occurrence of LRs, but inhibits the LRs’ length [32], which may be related to the concentration of NaHS used in the treatment.
The effect of H2S on the formation and growth of adventitious roots is the same as that for lateral roots. The application of the appropriate concentration of H2S promoted the number and length of adventitious roots in sweet potato [20][5]. In addition, the same result was obtained for excised willow, soybeans [20][5], and cucumber [21,22][6][7].

2. Hydrogen Sulfide Inhibits the Growth of Primary Roots and Root Hair

Several studies have shown that H2S has a toxic effect on the growth of primary roots. The concentration of exogenous NaHS used in treatments was negatively correlated with the rate of growth (length) of primary roots [28,29,32][8][9][10]. This inhibitory effect of H2S on primary roots may be related to the reduction in the meristem cell division potential, as the length of the root meristematic zones were reduced when treated with NaHS [28][8]. Although H2S inhibited the length of root meristematic zones, Li et al. [29][9] found that the length from the root apex to a root hair for the seedlings was promoted by H2S. This may be due to the inhibitory effect of H2S on root hairs. H2S is known to inhibit the initiation of root hair; that is, the starting site of the root hair zones may be further away from the root apex [29][9], resulting in a longer distance from the root hair to root apex, even when H2S inhibits the meristem zones. In addition, H2S not only inhibited the initiation of root hair growth, but also significantly decreased the root hair length and density [29][9].

3. Hydrogen Sulfide Promotes the Formation of Root Nodules and Nitrogen Fixation

Root nodules are a special organ formed by symbiosis between leguminous plants (Fabaceae) and rhizobia. The formation and growth of the nodules are strictly controlled by plant hormones [36][11]. As a recognized signal molecule that interacts with plant hormones to regulate plant growth and development, H2S is known to influence the growth of root nodules [30,31][12][13]. Endogenous H2S production in both young soybean nodules (14 days post-inoculation [DPI] with the Sinorhizobium fredii Q8 strain) and mature nodules (28 DPI) can be detected by fluorescent probes SF7-A, whereas no significant fluorescence was observed in the nascent soybean nodules (7 DPI). This suggested that H2S may mediate the growth of root nodules [31][13]. Indeed, the application of NaHS significantly increased the number of soybean nodules and enhanced nitrogenase (Nase) activity after 7 DPI and 24 DPI, respectively. In addition, H2S was found to affect rhizobial infection, where a greater abundance of developing infection threads and cortex infection threads was found in NaHS-treated soybean roots than those in untreated controls at 5 DPI and 7 DPI, respectively [30][12]. On the contrary, an endogenous H2S production deficit rhizobia mutant ΔCSE (cystathionine γ-lyase) symbiosis with soybean roots significantly reduced the nitrogenase activity and H2S content in nodule cells. Moreover, higher contents of H2O2 (hydrogen peroxide), MDA (malondialdehyde), and protein carbonyl were observed in ΔCSE root nodules; that is, the H2S-induced nitrogen-fixation ability of root nodules may be related to its regulation of the antioxidant system that protects nodule cells from oxidative damage [31][13]. These studies suggested that H2S might have a positive effect on the soybean–rhizobium symbiosis system and may enhance nitrogen fixation.

4. Hydrogen Sulfide Interacts with Other Signaling Molecules to Regulate Root Development

4.1. Auxin

The inhibition of primary root growth by H2S, and the promotion of lateral and adventitious root formation was consistent with the known effects of auxin on root development. It is not difficult to associate H2S and auxin signaling to RSA. The change in the endogenous IAA (indole acetic acid) content was similar to that reported for H2S, but with different time-courses in sweet potato explants. The increase in the H2S content during the formation of sweet potato adventitious roots preceded changes to the IAA content [20][5]. The research of Wu et al. (2021) [33][4] on peach roots also obtained similar results: NaHS induced a significant increase in the endogenous H2S content in roots at 1 DAT (days after treatment), while it increased the concentration of endogenous auxin in roots by 44.50% at 5 DAT. Moreover, it was found that treatment with NaHS significantly increased the production of IAA, and that N-1-naphthylphthalamic acid (an IAA transport inhibitor, NPA) weakened the effect of H2S on the number of adventitious roots in sweet potato, soybean, and willow [20][5]. These results showed that IAA may be located downstream of H2S in order to mediate root development. However, the results in tomato indicated H2S might partially act as a downstream component of the auxin signaling to trigger lateral root formation [23][1]. The depletion of auxin down-regulated the transcription of SlDES1 (L-cysteine desulfhydrase 1, a H2S synthesis gene), DES activity, and endogenous H2S contents in tomato roots, and the inhibitory effect of NPA on lateral root formation was offset by NaHS, whereas the inhibition of lateral root formation by HT was not reversed by naphthalene acetic acid (NAA) [23][1]. In addition, H2S not only induced auxin synthesis, but also affected the auxin response and transport. After the application of NaHS, the expression of the indicator of the auxin response DR5::GUS (synthetic auxin-responsive promoter::β-glucuronidase) was attenuated in the quiescent center (QC), columella initial cells, and mature columella cells of the root apex, and was concentrated to the QC [32][10]. The movement of auxin in the root acropetal and basipetal was reduced by an increase in the NaHS concentration, which implied that an increase in H2S levels reduces the IAA transport capacity. Further research showed that the inhibition of IAA transport by H2S was related to the polar subcellular localization of PIN proteins (PIN1, PIN2, PIN4, and PIN7) [32][10].

4.2. Reactive Oxygen Species

High concentrations of ROS (reactive oxygen species) often cause oxidative damage to plants, but low concentrations of ROS are necessary for signaling to maintain plant growth and development. The ROS-related regulation of root development has been reported for Arabidopsis [37][14], tomato [38][15], maize [39[16][17],40], and sweet potato [41][18]. The relationship between ROS and H2S for the regulation of root growth was also discussed in several studies [25,28,34][19][8][20]. These studies found that ROS signaling might be downstream of H2S to mediate RSA. For example, H2S could induce the expression of RBOH1 (respiratory burst oxidase 1) in tomato roots and could enhance the accumulation of H2O2, thereby promoting lateral root formation. These H2S-related effects on lateral roots were destroyed by DMTU (dimethylthiourea, a H2O2 scavenger) and DPI (diphenylene idonium, an inhibitor of NADPH oxidase) [25][19]. The inhibitory effect of H2S on primary root growth depended on the ROS pathway, as the relative root growth in rbohF and rbohD/F was higher than that in WT for the NaHS treatment, which meant that respiratory burst oxidase homolog mutants (rboh) were less sensitive to treatment with NaHS [28][8]. The promoting effect of H2S on strawberry roots during plug transplant production could also be attributed (in part) to the elevated H2O2 [34][20].

4.3. Nitric Oxide and Carbon Monoxide

Nitric oxide (NO), carbon monoxide (CO), and H2S are the three gas signal molecules in organisms. NO and CO also participate in root growth and development [42,43,44,45,46,47][21][22][23][24][25][26]. Therefore, the relationship between H2S and NO or CO has attracted attention in the regulation of RSA. The H2S-mediated adventitious root formation was alleviated by 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO, an NO scavenger) in sweet potato, willow, and soybean [20][5]. The toxic effect of H2S on the primary root of Arabidopsis was reduced in NO synthase mutants (nia1/2 and noa1), or when treated with cPTIO and NG-nitro-L-Arg-methyl ester (L-NAME, NO synthesis inhibitor) [28][8]. These results indicated that H2S acts upstream of NO signal transduction pathways when regulating adventitious root formation and primary root growth. From the results reported by Lin et al. (2012) [21][6], it is known that haem oxygenase-1/carbon monoxide (HO-1/CO) also acts as a downstream signal system during H2S-induced adventitious root formation. NaHS up-regulated HO1 gene expression and promoted HO1 protein accumulation, thereby increasing the number of cucumber adventitious roots. These phenomena were inhibited by ZnPPIX (zinc protoporphyrin IX, an inhibitor of HO-1), whereas the removal of H2S by HT did not affect the CO-induced adventitious rooting.

4.4. Brassinosteroid, Methane, and Cinnamaldehyde

Brassinosteroid (BR) contributes to the maintenance of root meristems, root cell elongation, lateral root development, root hair formation, and rhizosphere symbiosis [48,49,50,51][27][28][29][30]. At present, there is no direct evidence that H2S interacts with BR to regulate root development, but a recent proteomic analysis in Kandelia obovata has shown that H2S induced the accumulation of the BR-positive regulator protein BSK [27][2]. An RNA-seq analysis also showed that differentially expressed genes (DEGs) in peach roots, regulated by H2S, were significantly enriched in the “Brassinosteroid biosynthesis” pathway [33][4]. These results implied that H2S-mediated RSA might depend on the BR signal pathway.
Methane (CH4) plays an important role in the response to abiotic stress (such as heavy metal, salinity, and osmotic stress) [52][31]. In recent years, the role of CH4 in the formation of lateral and adventitious roots has been elucidated [22,26,53,54,55,56][7][32][33][34][35][36]. Both NO and CO signaling pathways were involved in CH4-induced adventitious root formation in cucumber [53,54][33][34]. Hydrogen peroxide (H2O2) signaling is also known to mediate the effects of CH4 on tomato lateral root formation [56][36]. As expected, H2S was confirmed to be located downstream of CH4 in order to regulate adventitious and lateral root formation in both cucumber and tomato. Methane induced the DES enzyme activity and promoted the production of endogenous H2S. These methane-related effects on the adventitious roots of cucumber were blocked by HT [22][7]. The same results were reported for the relationship between CH4 and H2S on the formation of lateral roots in tomato [26][32].
Cinnamaldehyde (CA) is a natural plant essential oil with antibacterial properties. It is widely used as a food additive and in medicines [57][37]. Recently, CA has also been used as a biological agent for plant disease resistance. For example, CA showed significant antibacterial activity against Pseudomonas syringae pv. actinidiae, which causes bacterial canker disease in kiwifruit [58][38]. Cinnamaldehyde reduced the number of Meloidogyne incognita galls and eggs on the roots of soybean plants to approximately 14% and 7%, respectively [59][39]. In addition, CA was found to play an important role in root development, as it markedly induced the formation of lateral roots in pepper, but without any inhibitory effect on primary root growth. Further study showed that H2S participated in this regulation process. Cinnamaldehyde increased the DES activity and promoted endogenous H2S production, thereby increasing the number of lateral roots. However, treatment with HT counteracted the effect of CA on endogenous H2S and lateral roots [24][3].

5. The Genes Involved in Hydrogen Sulfide-Mediated Root Development

Root system architecture is continuously adjusted in response to changes in various endogenous and exogenous factors (such as plant hormones, light, nutrition, and water). The regulation of these factors on root development involves many genes, including genes related to auxin synthesis, transport, and response, and genes related to cytokinin, abscisic acid (ABA), nitrate sensing and transport, and photoreceptors. The roles of these genes in plant growth and development were reviewed by Satbhai et al. (2015) [60][40]. In addition, many miRNAs are also involved in root development and architecture [2][41]. It is therefore important for researchers to have a clear understanding of which genes are involved in H2S signaling, and hence the regulation of root development. WResearchers have carried out a detailed discussion and summary of gene regulation below.

5.1. Genes Associated with the Auxin Signaling Pathway

The RNA-seq results for peach roots showed that 963 and 1113 DEGs were detected after H2S treatments for 1 day and 5 days, respectively [33][4]. These DEGs were significantly enriched in the “Glutathione metabolism”, “Plant-pathogen interaction”, “Plant hormone signal transduction”, “Brassinosteroid biosynthesis”, and “Cyanoamino acid metabolism” pathways. In particular, the pathway for “Plant hormone signal transduction” was significantly enriched when treated with H2S for 1 day and 5 days. A significant proportion (73.68%) of the genes associated with this pathway were related to auxin. More specifically, there were 2, 7, and 17 genes involved in auxin biosynthesis, transport, and signal transduction, respectively. These auxin-related genes included UGT74B1, TAA1, PINs, ABCBs, ARFs, Aux/IAAs, GH3, and SAUR. The auxin-synthesis-related gene UGT74B1 was up-regulated 1.95-fold when subjected to the H2S treatment. This might explain the H2S-induced increase in the root auxin content [20,33][5][4]. PINs exhibited different expression patterns over time under the NaHS treatment. After treatment with NaHS, PIN1 was up-regulated during 3 to 6 h and recovered to the control levels by 6 h, and the expression of PIN2 and PIN7 increased during 3 to 6 h, whereas it decreased in 12 or 24 h. On the contrary, the expression of PIN4 decreased after being treated with NaHS for 3 to 12 h, but recovered by 24 h. Although H2S had different effects on the expression of the PIN genes, its effect on the subcellular distribution of the PIN proteins was consistent. H2S disrupted the polar distribution of the PIN proteins (PIN1, PIN2, PIN4, and PIN7) on the plasma membrane in the root epidermal cells, and a large amount of PIN::GFP signals were found to dissociate from the plasma membrane upon cytoplasmic entry. Therefore, H2S inhibited auxin transport through its effect on the polarity distribution of PIN proteins, thus promoting the initiation of lateral roots [32][10]. It has been noted that the location of PIN proteins on the membrane was affected by F-actin [61[42][43],62], while H2S significantly reduced the occupancy rate of F-actin bundles in each cell. This led to the disappearance of thick actin cables [32][10]. This implied that the influence of H2S on the distribution of PIN proteins depended on the actin cytoskeleton, which is directly controlled by different ABPs (actin-binding proteins) [63][44]. Therefore, the expression of ABPs (CPA, CBP, and PRF3) was found to be up-regulated by H2S, whereas the effects of H2S on the percentage occupancy of the F-actin bundles was partially removed in the cpa, cbp, and prf3 mutants [32][10]. In addition, some auxin signal transduction genes were found to be regulated by H2S during root development. CsAux22D-like and CsAux22B-like were up-regulated by H2S during the formation of cucumber adventitious roots [22][7]. Hydrogen sulfide induced miR390a and miR160, and thus inhibited the expression of their target genes ARF4 and ARF16 in both tomato and Arabidopsis roots [25,26][19][32]. AtGATA23 and AtLBD16 were down-regulated in the Atdes1 mutant compared to WT, whereas AtGH3.1 and AtIAA28 were up-regulated in the Atdes1 mutant [26][32].

5.2. Genes Associated with Cell Proliferation

Cell proliferation is the basis for root growth and development, so the expression of cell-proliferation-related genes is very important during root growth. In the tomato root, H2S up-regulated SlCDKA;1, SlCYCA2;1, and AtCYCA2;3, but down-regulated SlKRP2 and AtKRP2 [25,26][19][32]. These genes are involved in the cell cycle. DNAJ-1, a gene phase that specifically regulates the G2/M cell cycle, was significantly induced by H2S in cucumber roots [21,22][6][7]. In addition, the expression of CsCDC6 (a cell-division-related gene) also increased in response to the NaHS treatment [22][7]. Interestingly, these cell proliferation-related genes also responded to auxin, CO, and CH4, which are closely related to the H2S signaling pathway. From the results of the RNA-seq work on peach roots, researchers identified that three cyclin genes and thirteen cell wall formation and remodeling-related genes were regulated by H2S [33][4]. All three cyclin genes (LOC109950471, LOC18790988, and LOC18784990) were up-regulated by H2S. In contrast, the cell wall formation and remodeling-related genes showed different patterns of expression in response to the H2S treatment [33][4].

5.3. Transcription Factors and Protein Kinases

Both transcription factors (TFs) and protein kinases are regulatory genes that mediate plant growth and development. Wu et al. (2021) [33][4] found that 36 transcription factors in peach roots were regulated by H2S, including LBD, MYB, and the AP2/ERF family. The overexpression of the peach PpLBD16, which was induced by H2S, significantly increased the number of lateral roots in Arabidopsis, whereas the Arabidopsis mutant ldb16 and ldb18 showed a decrease in the number of lateral roots [64][45]. These results strengthened ourthe understanding of LBD-mediated lateral root growth. Interestingly, LBDs (such as AtLBD16, AtLBD18, and AtLBD29) have been shown to be directly regulated by ARFs when regulating the formation of lateral roots [65,66][46][47], which implies that H2S may interact with the auxin signaling pathway to regulate the growth of lateral roots, partly dependent on LBD genes. In Kandelia obovata roots, other TFs were also found to respond to H2S, such as trihelix transcription factor GT-3b (GT-3B), the zinc finger CCCH domain-containing protein 14 (ZC3H14), and the MADS-box transcription factor [27][2].
Previous studies have shown that several protein kinases respond to H2S during root development. The calmodulin kinases CsCDPK1 and CsCDPK5 were up-regulated by H2S in cucumber roots [21][6]. MPK6 was involved in H2S-inhibited primary root growth. When subjected to the NaHS treatment, the root length of the mutant mpk6 was significantly longer than that for WT. Moreover, MPK6 was shown to function downstream of H2S-induced ROS and upstream of NO [35][48]. In addition, in peach roots, the DEGs in the H2S treatment for five days were significantly enriched in the mitogen-activated protein kinase (MAPK) signaling pathway, relative to the control group [33][4]. These results suggested that CDPK and MAPK may play an important role in H2S-regulated root development.

5.4. Genes Associated with Carbohydrate Metabolism

Hu et al. (2020) [34][20] reported that H2S induced the accumulation of soluble sugar in strawberry roots during plug production. Subsequently, the transcriptome and proteome data showed that the H2S-regulated genes in roots were significantly enriched in “Starch and sucrose metabolism” [27,33][2][4]. These data indicated that soluble sugar was either directly or indirectly involved with H2S-regulated root development. The sucrose transport protein SUT13, bidirectional sugar transporter SWEET, and invertase (INV) were found to be up-regulated by H2S in Kandelia obovata roots, which led researchers to speculate that H2S may facilitate sucrose transport and promote the hydrolysis of sucrose to provide metabolites and energy for root growth.

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